Skip to main content
SpringerLink
Log in

Collagens as New Players in Nervous System Diseases

  • Chapter
  • First Online:
The Collagen Superfamily and Collagenopathies

Part of the book series: Biology of Extracellular Matrix ((BEM,volume 8))

Abstract

The binomial nervous system involves the central nervous system (CNS), comprising the brain and the spinal cord, and the peripheral nervous system (PNS). Both divisions of the nervous system contain electrically excitable neurons as well as a number of supporting neuroglial cells, which include oligodendrocytes, astrocytes, microglia, choroid plexus ependymal cells in the CNS, and satellite and Schwann cells in the PNS. Connective tissues rich in fibrillar collagens form the outermost cover for the nervous system proper. Moreover, there are rich basement membranes (BM) surrounding all nervous system tissues and vessels within these structures. BMs compartmentalize nervous tissues and contribute to selective barrier and filtration functions essential for brain homeostasis. While BMs are absent from the brain parenchyma, there are extracellular matrices (ECM) in these regions that remain under-explored. The composition and types of matrices differ substantially in different parts of the nervous system. ECMs are significantly abundant during development, guiding cellular migration and differentiation as well as axon navigation and synaptogenesis. Additionally, ECMs promote neuronal health, contribute to synaptic homeostasis and plasticity, and are upregulated in response to disease and trauma. It is for these reasons that the mutation and malfunction of collagens have been linked to neurodevelopmental, degenerative, and psychiatric disorders as well as motor and sensory dysfunction. In recent years, it has become clear that collagens, constituting a major family of ECM proteins, and other extracellular components are generated not only by glial cells but also by neurons. The functions and expression patterns of the collagen superfamily members in the nervous system are summarized in this chapter, where we focus on their roles in vitro and in vivo in a number of animal models, and in human diseases of the nervous system.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

Aβ:

Amyloid beta

AChR:

Acetylcholine receptor

AD:

Alzheimer’s disease

ALS:

Amyotrophic lateral sclerosis

APP:

Amyloid precursor protein

BBB:

Blood–brain barrier

BM:

Basement membrane

BP:

Bullous pemphigoid

COL:

Collagenous domain

CLAC:

Collagen-like Alzheimer amyloid plaque component

CLAC-P:

CLAC precursor

CNS:

Central nervous system

CMS:

Congenital myasthenic syndrome

DDR:

Discoidin domain receptor

DRG:

Dorsal root ganglion

ECM:

Extracellular matrix

FACIT:

Fibril-associated collagens with interrupted triple helices

MACIT:

Membrane-associated collagens with interrupted triple helices

Multiplexin:

Multiple triple-helix domains with interruptions

NC:

Non-collagenous domain

NMJ:

Neuromuscular junction

PNN:

Perineuronal net

PNS:

Peripheral nervous system

PTP:

Protein tyrosine phosphatase

ROS:

Reactive oxygen species

SVCT2:

Sodium-dependent vitamin C transporter 2

References

  • Ackley BD, Crew JR, Elamaa H, Pihlajaniemi T, Kuo CJ, Kramer JM (2001) The NC1/endostatin domain of Caenorhabditis elegans type XVIII collagen affects cell migration and axon guidance. J Cell Biol 152:1219–1232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ackley BD, Kang SH, Crew JR, Suh C, Jin Y, Kramer JM (2003) The basement membrane components nidogen and type XVIII collagen regulate organization of neuromuscular junctions in Caenorhabditis elegans. J Neurosci 23:3577–3587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allen JM, Zamurs L, Brachvogel B, Schlotzer-Schrehardt U, Hansen U, Lamande SR, Rowley L, Fitzgerald J, Bateman JF (2009) Mice lacking the extracellular matrix protein WARP develop normally but have compromised peripheral nerve structure and function. J Biol Chem 284:12020–12030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amber KT, Zikry J, Hertl M (2017) A multi-hit hypothesis of bullous pemphigoid and associated neurological disease: is HLA-DQB1*03:01, a potential link between immune privileged antigen exposure and epitope spreading? HLA 89:127–134

    Article  CAS  PubMed  Google Scholar 

  • An JH, Lee SY, Jeon JY, Cho KG, Kim SU, Lee MA (2009) Identification of gliotropic factors that induce human stem cell migration to malignant tumor. J Proteome Res 8:2873–2881

    Article  CAS  PubMed  Google Scholar 

  • Andrikopoulos K, Suzuki HR, Solursh M, Ramirez F (1992) Localization of pro-alpha 2(V) collagen transcripts in the tissues of the developing mouse embryo. Dev Dyn 195:113–120

    Article  CAS  PubMed  Google Scholar 

  • Aricescu AR, McKinnell IW, Halfter W, Stoker AW (2002) Heparan sulfate proteoglycans are ligands for receptor protein tyrosine phosphatase sigma. Mol Cell Biol 22:1881–1892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Banerjee S, Isaacman-Beck J, Schneider VA, Granato M (2013) A novel role for Lh3 dependent ECM modifications during neural crest cell migration in zebrafish. PLoS One 8:e54609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bastuji-Garin S, Joly P, Lemordant P, Sparsa A, Bedane C, Delaporte E, Roujeau JC, Bernard P, Guillaume JC, Ingen-Housz-Oro S, Maillard H, Pauwels C, Picard-Dahan C, Dutronc Y, Richard MA, French Study Group for Bullous Diseases (2011) Risk factors for bullous pemphigoid in the elderly: a prospective case-control study. J Invest Dermatol 131:637–643

    Google Scholar 

  • Bauer R, Ratzinger S, Wales L, Bosserhoff A, Senner V, Grifka J, Grassel S (2011) Inhibition of collagen XVI expression reduces glioma cell invasiveness. Cell Physiol Biochem 27:217–226

    Article  CAS  PubMed  Google Scholar 

  • Beattie CE, Melancon E, Eisen JS (2000) Mutations in the stumpy gene reveal intermediate targets for zebrafish motor axons. Development 127:2653–2662

    Article  CAS  PubMed  Google Scholar 

  • Bedal KB, Grassel S, Oefner PJ, Reinders J, Reichert TE, Bauer R (2014) Collagen XVI induces expression of MMP9 via modulation of AP-1 transcription factors and facilitates invasion of oral squamous cell carcinoma. PLoS One 9:e86777

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Birk DE, Fitch JM, Babiarz JP, Doane KJ, Linsenmayer TF (1990) Collagen fibrillogenesis in vitro: interaction of types I and V collagen regulates fibril diameter. J Cell Sci 95(Pt 4):649–657

    Article  CAS  PubMed  Google Scholar 

  • Booth BA, Uitto J (1981) Collagen biosynthesis by human skin fibroblasts. III. The effects of ascorbic acid on procollagen production and prolyl hydroxylase activity. Biochim Biophys Acta 675:117–122. 0304-4165(81)90076-3 [pii]

    Google Scholar 

  • Boot-Handford RP, Tuckwell DS, Plumb DA, Rock CF, Poulsom R (2003) A novel and highly conserved collagen (pro(alpha)1(XXVII)) with a unique expression pattern and unusual molecular characteristics establishes a new clade within the vertebrate fibrillar collagen family. J Biol Chem 278:31067–31077

    Article  CAS  PubMed  Google Scholar 

  • Breedveld G, de Coo IF, Lequin MH, Arts WF, Heutink P, Gould DB, John SW, Oostra B, Mancini GM (2006) Novel mutations in three families confirm a major role of COL4A1 in hereditary porencephaly. J Med Genet 43:490–495. jmg.2005.035584 [pii]

    Google Scholar 

  • Bretaud S, Pagnon-Minot A, Guillon E, Ruggiero F, Le Guellec D (2011) Characterization of spatial and temporal expression pattern of Col15a1b during zebrafish development. Gene Expr Patterns 11:129–134

    Article  CAS  PubMed  Google Scholar 

  • Bretaud S, Guillon E, Karppinen S, Pihlajaniemi T, Ruggiero F (2020) Collagen XV, a multifaceted multiplexin present across tissues and species. Matrix Biol Plus 6–7

    Google Scholar 

  • Brick KE, Weaver CH, Savica R, Lohse CM, Pittelkow MR, Boeve BF, Gibson LE, Camilleri MJ, Wieland CN (2014) A population-based study of the association between bullous pemphigoid and neurologic disorders. J Am Acad Dermatol 71:1191–1197

    Article  PubMed  PubMed Central  Google Scholar 

  • Bunge MB, Williams AK, Wood PM, Uitto J, Jeffrey JJ (1980) Comparison of nerve cell and nerve cell plus Schwann cell cultures, with particular emphasis on basal lamina and collagen formation. J Cell Biol 84:184–202

    Article  CAS  PubMed  Google Scholar 

  • Caglayan AO, Baranoski JF, Aktar F, Han W, Tuysuz B, Guzel A, Guclu B, Kaymakcalan H, Aktekin B, Akgumus GT, Murray PB, Erson-Omay EZ, Caglar C, Bakircioglu M, Sakalar YB, Guzel E, Demir N, Tuncer O, Senturk S, Ekici B, Minja FJ, Sestan N, Yasuno K, Bilguvar K, Caksen H, Gunel M (2014) Brain malformations associated with Knobloch syndrome—review of literature, expanding clinical spectrum, and identification of novel mutations. Pediatr Neurol 51:806–813.e8

    Article  PubMed  PubMed Central  Google Scholar 

  • Cai SC, Allen JC, Lim YL, Chua SH, Tan SH, Tang MB (2014) Mortality of bullous pemphigoid in Singapore: risk factors and causes of death in 359 patients seen at the National Skin Centre. Br J Dermatol 170:1319–1326

    Article  CAS  PubMed  Google Scholar 

  • Calvo AC, Cibreiro GA, Merino PT, Roy JF, Galiana A, Rufian AJ, Cano JM, Martin MA, Moreno L, Larrode P, Vazquez PC, Galan L, Mora J, Munoz-Blanco JL, Munoz MJ, Zaragoza P, Pegoraro E, Soraru G, Mora M, Lunetta C, Penco S, Tarlarini C, Esteban J, Osta R, Redondo AG (2019) Collagen XIX alpha 1 improves prognosis in amyotrophic lateral sclerosis. Aging Dis 10:278–292

    Article  PubMed  PubMed Central  Google Scholar 

  • Carey DJ, Eldridge CF, Cornbrooks CJ, Timpl R, Bunge RP (1983) Biosynthesis of type IV collagen by cultured rat Schwann cells. J Cell Biol 97:473–479

    Article  CAS  PubMed  Google Scholar 

  • Carlson SS, Valdez G, Sanes JR (2010) Presynaptic calcium channels and alpha3-integrins are complexed with synaptic cleft laminins, cytoskeletal elements and active zone components. J Neurochem 115:654–666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cescon M, Chen P, Castagnaro S, Gregorio I, Bonaldo P (2016) Lack of collagen VI promotes neurodegeneration by impairing autophagy and inducing apoptosis during aging. Aging (Albany NY) 8:1083–1101

    Article  CAS  Google Scholar 

  • Cescon M, Gregorio I, Eiber N, Borgia D, Fusto A, Sabatelli P, Scorzeto M, Megighian A, Pegoraro E, Hashemolhosseini S, Bonaldo P (2018) Collagen VI is required for the structural and functional integrity of the neuromuscular junction. Acta Neuropathol 136:483

    Article  CAS  PubMed  Google Scholar 

  • Charnas LR, Marini JC (1995) Neurologic profile in osteogenesis imperfecta. Connect Tissue Res 31:23

    Article  Google Scholar 

  • Charsar BA, Goldberg EM (2017) Polymicrogyria and intractable epilepsy in siblings with Knobloch syndrome and homozygous mutation of COL18A1. Pediatr Neurol 76:91–92. S0887-8994(17)30804-4 [pii]

    Google Scholar 

  • Cheah KS, Lau ET, Au PK, Tam PP (1991) Expression of the mouse alpha 1(II) collagen gene is not restricted to cartilage during development. Development 111:945–953

    Article  CAS  PubMed  Google Scholar 

  • Chen ZL, Strickland S (2003) Laminin gamma1 is critical for Schwann cell differentiation, axon myelination, and regeneration in the peripheral nerve. J Cell Biol 163:889–899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen P, Cescon M, Megighian A, Bonaldo P (2014) Collagen VI regulates peripheral nerve myelination and function. FASEB J 28:1145–1156

    Article  CAS  PubMed  Google Scholar 

  • Cheng JS, Dubal DB, Kim DH, Legleiter J, Cheng IH, Yu GQ, Tesseur I, Wyss-Coray T, Bonaldo P, Mucke L (2009) Collagen VI protects neurons against Abeta toxicity. Nat Neurosci 12:119–121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng IH, Lin YC, Hwang E, Huang HT, Chang WH, Liu YL, Chao CY (2011) Collagen VI protects against neuronal apoptosis elicited by ultraviolet irradiation via an Akt/phosphatidylinositol 3-kinase signaling pathway. Neuroscience 183:178–188

    Article  CAS  PubMed  Google Scholar 

  • Chernousov MA, Stahl RC, Carey DJ (1998) Schwann cells use a novel collagen-dependent mechanism for fibronectin fibril assembly. J Cell Sci 111(Pt 18):2763–2777

    Article  CAS  PubMed  Google Scholar 

  • Chernousov MA, Rothblum K, Tyler WA, Stahl RC, Carey DJ (2000) Schwann cells synthesize type V collagen that contains a novel alpha 4 chain. Molecular cloning, biochemical characterization, and high affinity heparin binding of alpha 4(V) collagen. J Biol Chem 275:28208–28215

    Google Scholar 

  • Chernousov MA, Stahl RC, Carey DJ (2001) Schwann cell type V collagen inhibits axonal outgrowth and promotes Schwann cell migration via distinct adhesive activities of the collagen and noncollagen domains. J Neurosci 21:6125–6135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chernousov MA, Rothblum K, Stahl RC, Evans A, Prentiss L, Carey DJ (2006) Glypican-1 and alpha4(V) collagen are required for Schwann cell myelination. J Neurosci 26:508–517

    Google Scholar 

  • Chernousov MA, Yu WM, Chen ZL, Carey DJ, Strickland S (2008) Regulation of Schwann cell function by the extracellular matrix. Glia 56:1498–1507

    Article  PubMed  Google Scholar 

  • Chosidow O, Doppler V, Bensimon G, Joly P, Salachas F, Lacomblez L, Prost C, Camu W, Frances C, Herson S, Meininger V (2000) Bullous pemphigoid and amyotrophic lateral sclerosis: a new clue for understanding the bullous disease? Arch Dermatol 136:521–524

    Article  CAS  PubMed  Google Scholar 

  • Christov A, Ottman J, Hamdheydari L, Grammas P (2008) Structural changes in Alzheimer’s disease brain microvessels. Curr Alzheimer Res 5:392–395

    Article  CAS  PubMed  Google Scholar 

  • Clementz AG, Mutolo MJ, Leir SH, Morris KJ, Kucybala K, Harris H, Harris A (2013) Collagen XV inhibits epithelial to mesenchymal transition in pancreatic adenocarcinoma cells. PLoS One 8:e72250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corbett MA, Turner SJ, Gardner A, Silver J, Stankovich J, Leventer RJ, Derry CP, Carroll R, Ha T, Scheffer IE, Bahlo M, Jackson GD, Mackey DA, Berkovic SF, Gecz J (2017) Familial epilepsy with anterior polymicrogyria as a presentation of COL18A1 mutations. Eur J Med Genet 60:437–443

    Article  PubMed  Google Scholar 

  • Court FA, Gillingwater TH, Melrose S, Sherman DL, Greenshields KN, Morton AJ, Harris JB, Willison HJ, Ribchester RR (2008) Identity, developmental restriction and reactivity of extralaminar cells capping mammalian neuromuscular junctions. J Cell Sci 121:3901–3911

    Article  CAS  PubMed  Google Scholar 

  • D’Antonio M, Michalovich D, Paterson M, Droggiti A, Woodhoo A, Mirsky R, Jessen KR (2006) Gene profiling and bioinformatic analysis of Schwann cell embryonic development and myelination. Glia 53:501–515

    Article  PubMed  Google Scholar 

  • Dhungana H, Huuskonen MT, Pihlajaniemi T, Heljasvaara R, Vivien D, Kanninen KM, Malm T, Koistinaho J, Lemarchant S (2017) Lack of collagen XV is protective after ischemic stroke in mice. Cell Death Dis 8:e2541

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Di Rosa M, Sanfilippo C, Libra M, Musumeci G, Malaguarnera L (2015) Different pediatric brain tumors are associated with different gene expression profiling. Acta Histochem 117:477–485

    Article  PubMed  CAS  Google Scholar 

  • Dusl M, Moreno T, Munell F, Macaya A, Gratacos M, Abicht A, Strom TM, Lochmuller H, Senderek J (2019) Congenital myasthenic syndrome caused by novel COL13A1 mutations. J Neurol 266:1107–1112

    Article  CAS  PubMed  Google Scholar 

  • Dziadek M, Timpl R (1985) Expression of nidogen and laminin in basement membranes during mouse embryogenesis and in teratocarcinoma cells. Dev Biol 111:372–382

    Article  CAS  PubMed  Google Scholar 

  • Dziadek M, Darling P, Bakker M, Overall M, Zhang RZ, Pan TC, Tillet E, Timpl R, Chu ML (1996) Deposition of collagen VI in the extracellular matrix during mouse embryogenesis correlates with expression of the alpha 3(VI) subunit gene. Exp Cell Res 226:302–315

    Article  CAS  PubMed  Google Scholar 

  • Eble JA, Kassner A, Niland S, Morgelin M, Grifka J, Grassel S (2006) Collagen XVI harbors an integrin alpha1 beta1 recognition site in its C-terminal domains. J Biol Chem 281:25745–25756

    Google Scholar 

  • Eklund L, Piuhola J, Komulainen J, Sormunen R, Ongvarrasopone C, Fässler R, Muona A, Ilves M, Ruskoaho H, Takala TE, Pihlajaniemi T (2001) Lack of type XV collagen causes a skeletal myopathy and cardiovascular defects in mice. Proc Natl Acad Sci USA 98:1194–1199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eldridge CF, Bunge MB, Bunge RP, Wood PM (1987) Differentiation of axon-related Schwann cells in vitro. I. Ascorbic acid regulates basal lamina assembly and myelin formation. J Cell Biol 105:1023–1034

    Article  CAS  PubMed  Google Scholar 

  • Eldridge CF, Bunge MB, Bunge RP (1989) Differentiation of axon-related Schwann cells in vitro: II. Control of myelin formation by basal lamina. J Neurosci 9:625–638

    Google Scholar 

  • Emery SC, Karpinski NC, Hansen L, Masliah E (1999) Abnormalities in central nervous system development in osteogenesis imperfecta type II. Pediatr Dev Pathol 2:124–130

    Article  CAS  PubMed  Google Scholar 

  • Ethell IM, Ethell DW (2007) Matrix metalloproteinases in brain development and remodeling: synaptic functions and targets. J Neurosci Res 85:2813–2823

    Article  CAS  PubMed  Google Scholar 

  • Favor J, Gloeckner CJ, Janik D, Klempt M, Neuhauser-Klaus A, Pretsch W, Schmahl W, Quintanilla-Fend L (2007) Type IV procollagen missense mutations associated with defects of the eye, vascular stability, the brain, kidney function and embryonic or postnatal viability in the mouse, Mus musculus: an extension of the Col4a1 allelic series and the identification of the first two Col4a2 mutant alleles. Genetics 175:725–736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrer-Ferrer M, Dityatev A (2018) Shaping synapses by the neural extracellular matrix. Front Neuroanat 12:40

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Forsell C, Björk BF, Lilius L, Axelman K, Fabre SF, Fratiglioni L, Winblad B, Graff C (2010) Genetic association to the amyloid plaque associated protein gene COL25A1 in Alzheimer’s disease. Neurobiol Aging 31:409–415

    Article  CAS  PubMed  Google Scholar 

  • Foureur N, Descamps V, Lebrun-Vignes B, Picard-Dahan C, Grossin M, Belaich S, Crickx B (2001) Bullous pemphigoid in a leg affected with hemiparesia: a possible relation of neurological diseases with bullous pemphigoid? Eur J Dermatol 11:230–233

    CAS  PubMed  Google Scholar 

  • Fox MA (2008) Novel roles for collagens in wiring the vertebrate nervous system. Curr Opin Cell Biol 20:508–513

    Article  CAS  PubMed  Google Scholar 

  • Fox MA, Sanes JR, Borza DB, Eswarakumar VP, Fässler R, Hudson BG, John SW, Ninomiya Y, Pedchenko V, Pfaff SL, Rheault MN, Sado Y, Segal Y, Werle MJ, Umemori H (2007) Distinct target-derived signals organize formation, maturation, and maintenance of motor nerve terminals. Cell 129:179–193

    Article  CAS  PubMed  Google Scholar 

  • Franzke CW, Bruckner P, Bruckner-Tuderman L (2005) Collagenous transmembrane proteins: recent insights into biology and pathology. J Biol Chem 280:4005–4008

    Article  CAS  PubMed  Google Scholar 

  • Frischknecht R, Gundelfinger ED (2012) The brain’s extracellular matrix and its role in synaptic plasticity. Adv Exp Med Biol 970:153–171

    Article  CAS  PubMed  Google Scholar 

  • Fujita A, Sato JR, Festa F, Gomes LR, Oba-Shinjo SM, Marie SK, Ferreira CE, Sogayar MC (2008) Identification of COL6A1 as a differentially expressed gene in human astrocytomas. Genet Mol Res 7:371–378

    Article  CAS  PubMed  Google Scholar 

  • Gal J, Chen J, Katsumata Y, Fardo DW, Wang WX, Artiushin S, Price D, Anderson S, Patel E, Zhu H, Nelson PT (2018) Detergent insoluble proteins and inclusion body-like structures immunoreactive for PRKDC/DNA-PK/DNA-PKcs, FTL, NNT, and AIFM1 in the amygdala of cognitively impaired elderly persons. J Neuropathol Exp Neurol 77:21–39

    Article  CAS  PubMed  Google Scholar 

  • Gara SK, Grumati P, Urciuolo A, Bonaldo P, Kobbe B, Koch M, Paulsson M, Wagener R (2008) Three novel collagen VI chains with high homology to the alpha3 chain. J Biol Chem 283:10658–10670

    Article  CAS  PubMed  Google Scholar 

  • Gatseva A, Sin YY, Brezzo G, Van Agtmael T (2019) Basement membrane collagens and disease mechanisms. Essays Biochem 63:297–312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gess B, Rohr D, Fledrich R, Sereda MW, Kleffner I, Humberg A, Nowitzki J, Strecker JK, Halfter H, Young P (2011) Sodium-dependent vitamin C transporter 2 deficiency causes hypomyelination and extracellular matrix defects in the peripheral nervous system. J Neurosci 31:17180–17192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goncalves TJM, Boutillon F, Lefebvre S, Goffin V, Iwatsubo T, Wakabayashi T, Oury F, Armand AS (2019) Collagen XXV promotes myoblast fusion during myogenic differentiation and muscle formation. Sci Rep 9:5878–5876

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gordon MK, Hahn RA (2010) Collagens. Cell Tissue Res 339:247–257

    Article  CAS  PubMed  Google Scholar 

  • Gould DB, Phalan FC, Breedveld GJ, van Mil SE, Smith RS, Schimenti JC, Aguglia U, van der Knaap, M S, Heutink P, John SW (2005) Mutations in Col4a1 cause perinatal cerebral hemorrhage and porencephaly. Science 308:1167–1171

    Google Scholar 

  • Gregorio I, Braghetta P, Bonaldo P, Cescon M (2018) Collagen VI in healthy and diseased nervous system. Dis Model Mech 11

    Google Scholar 

  • Grimal S, Puech S, Wagener R, Venteo S, Carroll P, Fichard-Carroll A (2010) Collagen XXVIII is a distinctive component of the peripheral nervous system nodes of ranvier and surrounds nonmyelinating glial cells. Glia 58:1977–1987

    Article  PubMed  Google Scholar 

  • Guillon E, Bretaud S, Ruggiero F (2016) Slow muscle precursors lay down a collagen XV matrix fingerprint to guide motor axon navigation. J Neurosci 36:2663–2676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hägg P, Rehn M, Huhtala P, Väisänen T, Tamminen M, Pihlajaniemi T (1998) Type XIII collagen is identified as a plasma membrane protein. J Biol Chem 273:15590–15597

    Article  PubMed  Google Scholar 

  • Hägg P, Väisänen T, Tuomisto A, Rehn M, Tu H, Huhtala P, Eskelinen S, Pihlajaniemi T (2001) Type XIII collagen: a novel cell adhesion component present in a range of cell-matrix adhesions and in the intercalated discs between cardiac muscle cells. Matrix Biol 19:727–742

    Article  PubMed  Google Scholar 

  • Haghighi A, Tiwari A, Piri N, Nurnberg G, Saleh-Gohari N, Haghighi A, Neidhardt J, Nurnberg P, Berger W (2014) Homozygosity mapping and whole exome sequencing reveal a novel homozygous COL18A1 mutation causing Knobloch syndrome. PLoS One 9:e112747

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Halfter W, Dong S, Schurer B, Cole GJ (1998) Collagen XVIII is a basement membrane heparan sulfate proteoglycan. J Biol Chem 273:25404–25412

    Article  CAS  PubMed  Google Scholar 

  • Härönen H, Zainul Z, Tu H, Naumenko N, Sormunen R, Miinalainen I, Shakirzyanova A, Oikarainen T, Abdullin A, Martin P, Santoleri S, Koistinaho J, Silman I, Giniatullin R, Fox MA, Heikkinen A, Pihlajaniemi T (2017) Collagen XIII secures pre- and postsynaptic integrity of the neuromuscular synapse. Hum Mol Genet 26:2076–2090

    Article  PubMed  CAS  Google Scholar 

  • Härönen H, Zainul Z, Naumenko N, Sormunen R, Miinalainen I, Shakirzyanova A, Santoleri S, Kemppainen AV, Giniatullin R, Pihlajaniemi T, Heikkinen A (2019) Correct expression and localization of collagen XIII are crucial for the normal formation and function of the neuromuscular system. Eur J Neurosci 49:1491–1511

    Article  PubMed  Google Scholar 

  • Hartmann D, Ziegenhagen MW, Sievers J (1998) Meningeal cells stimulate neuronal migration and the formation of radial glial fascicles from the cerebellar external granular layer. Neurosci Lett 244:129–132

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto T, Wakabayashi T, Watanabe A, Kowa H, Hosoda R, Nakamura A, Kanazawa I, Arai T, Takio K, Mann DM, Iwatsubo T (2002) CLAC: a novel Alzheimer amyloid plaque component derived from a transmembrane precursor, CLAC-P/collagen type XXV. EMBO J 21:1524–1534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayashi G, Labelle-Dumais C, Gould DB (2018) Use of sodium 4-phenylbutyrate to define therapeutic parameters for reducing intracerebral hemorrhage and myopathy in Col4a1 mutant mice. Dis Model Mech 11

    Google Scholar 

  • Heck N, Garwood J, Schutte K, Fawcett J, Faissner A (2003) Astrocytes in culture express fibrillar collagen. Glia 41:382–392

    Article  PubMed  Google Scholar 

  • Heikkinen A, Tu H, Pihlajaniemi T (2012) Collagen XIII: a type II transmembrane protein with relevance to musculoskeletal tissues, microvessels and inflammation. Int J Biochem Cell Biol 44:714–717

    Google Scholar 

  • Heikkinen A, Härönen H, Norman O, Pihlajaniemi T (2020) Collagen XIII and other ECM components in the assembly and disease of the neuromuscular junction. Anat Rec (Hoboken)

    Google Scholar 

  • Heljasvaara R, Aikio M, Ruotsalainen H, Pihlajaniemi T (2017) Collagen XVIII in tissue homeostasis and dysregulation – lessons learned from model organisms and human patients. Matrix Biol 57–58:55–75

    Google Scholar 

  • Hilario JD, Wang C, Beattie CE (2010) Collagen XIXa1 is crucial for motor axon navigation at intermediate targets. Development 137:4261–4269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill R (2009) Extracellular matrix remodelling in human diabetic neuropathy. J Anat 214:219–225

    Article  PubMed  PubMed Central  Google Scholar 

  • Hirano S, Yonezawa T, Hasegawa H, Hattori S, Greenhill NS, Davis PF, Sage EH, Ninomiya Y (2004) Astrocytes express type VIII collagen during the repair process of brain cold injury. Biochem Biophys Res Commun 317:437–443

    Article  CAS  PubMed  Google Scholar 

  • Hubert T, Grimal S, Ratzinger S, Mechaly I, Grassel S, Fichard-Carroll A (2007) Collagen XVI is a neural component of the developing and regenerating dorsal root ganglia extracellular matrix. Matrix Biol 26:206–210

    Article  CAS  PubMed  Google Scholar 

  • Hubert T, Grimal S, Carroll P, Fichard-Carroll A (2009) Collagens in the developing and diseased nervous system. Cell Mol Life Sci 66:1223–1238

    Article  CAS  PubMed  Google Scholar 

  • Hurskainen T, Moilanen J, Sormunen R, Franzke CW, Soininen R, Löffek S, Huilaja L, Nuutinen M, Bruckner-Tuderman L, Autio-Harmainen H, Tasanen K (2012) Transmembrane collagen XVII is a novel component of the glomerular filtration barrier. Cell Tissue Res 348:579–588

    Article  CAS  PubMed  Google Scholar 

  • Ishihara E, Takahashi S, Fukaya R, Ohta S, Yoshida K, Toda M (2019) Identification of KLRC2 as a candidate marker for brain tumor-initiating cells. Neurol Res 41:1043–1049

    Article  CAS  PubMed  Google Scholar 

  • Jacków J, Löffek S, Nyström A, Bruckner-Tuderman L, Franzke CW (2016a) Collagen XVII shedding suppresses re-epithelialization by directing keratinocyte migration and dampening mTOR signaling. J Invest Dermatol 136:1031–1041

    Article  PubMed  CAS  Google Scholar 

  • Jacków J, Schlosser A, Sormunen R, Nyström A, Sitaru C, Tasanen K, Bruckner-Tuderman L, Franzke CW (2016b) Generation of a functional non-shedding collagen XVII mouse model: relevance of collagen XVII shedding in wound healing. J Invest Dermatol 136:516–525

    Article  PubMed  CAS  Google Scholar 

  • Jeanne M, Gould DB (2017) Genotype-phenotype correlations in pathology caused by collagen type IV alpha 1 and 2 mutations. Matrix Biol 57-58:29–44

    Article  CAS  PubMed  Google Scholar 

  • Jeanne M, Labelle-Dumais C, Jorgensen J, Kauffman WB, Mancini GM, Favor J, Valant V, Greenberg SM, Rosand J, Gould DB (2012) COL4A2 mutations impair COL4A1 and COL4A2 secretion and cause hemorrhagic stroke. Am J Hum Genet 90:91–101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeanne M, Jorgensen J, Gould DB (2015) Molecular and genetic analyses of collagen type IV mutant mouse models of spontaneous intracerebral hemorrhage identify mechanisms for stroke prevention. Circulation 131:1555–1565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jovanov Milosevic N, Judas M, Aronica E, Kostovic I (2014) Neural ECM in laminar organization and connectivity development in healthy and diseased human brain. Prog Brain Res 214:159–178

    Article  PubMed  Google Scholar 

  • Kakuyama H, Soderberg L, Horigome K, Winblad B, Dahlqvist C, Naslund J, Tjernberg LO (2005) CLAC binds to aggregated Abeta and Abeta fragments, and attenuates fibril elongation. Biochemistry 44:15602–15609

    Article  CAS  PubMed  Google Scholar 

  • Kamei A, Houdou S, Mito T, Konomi H, Takashima S (1992) Developmental change in type VI collagen in human cerebral vessels. Pediatr Neurol 8:183–186

    Article  CAS  PubMed  Google Scholar 

  • Kapoor R, Sakai LY, Funk S, Roux E, Bornstein P, Sage EH (1988) Type VIII collagen has a restricted distribution in specialized extracellular matrices. J Cell Biol 107:721–730

    Article  CAS  PubMed  Google Scholar 

  • Karkheiran S, Krebs CE, Makarov V, Nilipour Y, Hubert B, Darvish H, Frucht S, Shahidi GA, Buxbaum JD, Paisan-Ruiz C (2013) Identification of COL6A2 mutations in progressive myoclonus epilepsy syndrome. Hum Genet 132:275–283

    Article  CAS  PubMed  Google Scholar 

  • Katisko K, Kokkonen N, Kruger J, Hartikainen P, Koivisto AM, Helisalmi S, Korhonen VE, Kokki M, Tuusa J, Herukka SK, Solje E, Haapasalo A, Tasanen K, Remes AM (2018) The association between frontotemporal lobar degeneration and bullous pemphigoid. J Alzheimers Dis 66:743–750

    Article  CAS  PubMed  Google Scholar 

  • Kay JN, De la Huerta I, Kim IJ, Zhang Y, Yamagata M, Chu MW, Meister M, Sanes JR (2011) Retinal ganglion cells with distinct directional preferences differ in molecular identity, structure, and central projections. J Neurosci 31:7753–7762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keene DR, Engvall E, Glanville RW (1988) Ultrastructure of type VI collagen in human skin and cartilage suggests an anchoring function for this filamentous network. J Cell Biol 107:1995–2006

    Article  CAS  PubMed  Google Scholar 

  • Keren B, Suzuki OT, Gerard-Blanluet M, Bremond-Gignac D, Elmaleh M, Titomanlio L, Delezoide AL, Passos-Bueno MR, Verloes A (2007) CNS malformations in Knobloch syndrome with splice mutation in COL18A1 gene. Am J Med Genet A 143A:1514–1518

    Article  CAS  PubMed  Google Scholar 

  • Kerever A, Schnack J, Vellinga D, Ichikawa N, Moon C, Arikawa-Hirasawa E, Efird JT, Mercier F (2007) Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor fibroblast growth factor 2 from the extracellular milieu. Stem Cells 25:2146–2157

    Article  CAS  PubMed  Google Scholar 

  • Khaleduzzaman M, Sumiyoshi H, Ueki Y, Inoguchi K, Ninomiya Y, Yoshioka H (1997) Structure of the human type XIX collagen (COL19A1) gene, which suggests it has arisen from an ancestor gene of the FACIT family. Genomics 45:304–312

    Article  CAS  PubMed  Google Scholar 

  • Khoshnoodi J, Pedchenko V, Hudson BG (2008) Mammalian collagen IV. Microsc Res Tech 71:357–370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kibsgaard L, Rasmussen M, Lamberg A, Deleuran M, Olesen AB, Vestergaard C (2017) Increased frequency of multiple sclerosis among patients with bullous pemphigoid: a population-based cohort study on comorbidities anchored around the diagnosis of bullous pemphigoid. Br J Dermatol 176:1486–1491

    Article  CAS  PubMed  Google Scholar 

  • Kleppel MM, Santi PA, Cameron JD, Wieslander J, Michael AF (1989) Human tissue distribution of novel basement membrane collagen. Am J Pathol 134:813–825

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kliemann SE, Waetge RT, Suzuki OT, Passos-Bueno MR, Rosemberg S (2003) Evidence of neuronal migration disorders in Knobloch syndrome: clinical and molecular analysis of two novel families. Am J Med Genet A 119A:15–19

    Article  PubMed  Google Scholar 

  • Koch M, Veit G, Stricker S, Bhatt P, Kutsch S, Zhou P, Reinders E, Hahn RA, Song R, Burgeson RE, Gerecke DR, Mundlos S, Gordon MK (2006) Expression of type XXIII collagen mRNA and protein. J Biol Chem 281:21546–21557

    Article  CAS  PubMed  Google Scholar 

  • Kokkonen N, Herukka SK, Huilaja L, Kokki M, Koivisto AM, Hartikainen P, Remes AM, Tasanen K (2017) Increased levels of the bullous pemphigoid BP180 autoantibody are associated with more severe dementia in Alzheimer’s disease. J Invest Dermatol 137:71–76

    Article  CAS  PubMed  Google Scholar 

  • Korogod N, Petersen CC, Knott GW (2015) Ultrastructural analysis of adult mouse neocortex comparing aldehyde perfusion with cryo fixation. Elife 4

    Google Scholar 

  • Kowa H, Sakakura T, Matsuura Y, Wakabayashi T, Mann DM, Duff K, Tsuji S, Hashimoto T, Iwatsubo T (2004) Mostly separate distributions of CLAC- versus Abeta40- or thioflavin S-reactivities in senile plaques reveal two distinct subpopulations of beta-amyloid deposits. Am J Pathol 165:273–281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krishnaswamy VR, Benbenishty A, Blinder P, Sagi I (2019) Demystifying the extracellular matrix and its proteolytic remodeling in the brain: structural and functional insights. Cell Mol Life Sci 76:3229–3248

    Article  CAS  PubMed  Google Scholar 

  • Kummer TT, Misgeld T, Sanes JR (2006) Assembly of the postsynaptic membrane at the neuromuscular junction: paradigm lost. Curr Opin Neurobiol 16:74–82

    Article  CAS  PubMed  Google Scholar 

  • Kuo CJ, LaMontagne KR, Garcia-Cardena G, Ackley BD, Kalman D, Park S, Christofferson R, Kamihara J, Ding YH, Lo KM, Gillies S, Folkman J, Mulligan RC, Javaherian K (2001) Oligomerization-dependent regulation of motility and morphogenesis by the collagen XVIII NC1/endostatin domain. J Cell Biol 152:1233–1246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuo DS, Labelle-Dumais C, Mao M, Jeanne M, Kauffman WB, Allen J, Favor J, Gould DB (2014) Allelic heterogeneity contributes to variability in ocular dysgenesis, myopathy and brain malformations caused by Col4a1 and Col4a2 mutations. Hum Mol Genet 23:1709–1722

    Article  CAS  PubMed  Google Scholar 

  • Labelle-Dumais C, Dilworth DJ, Harrington EP, de Leau M, Lyons D, Kabaeva Z, Manzini MC, Dobyns WB, Walsh CA, Michele DE, Gould DB (2011) COL4A1 mutations cause ocular dysgenesis, neuronal localization defects, and myopathy in mice and Walker-Warburg syndrome in humans. PLoS Genet 7:e1002062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Labelle-Dumais C, Schuitema V, Hayashi G, Hoff K, Gong W, Dao DQ, Ullian EM, Oishi P, Margeta M, Gould DB (2019) COL4A1 mutations cause neuromuscular disease with tissue-specific mechanistic heterogeneity. Am J Hum Genet 104:847–860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lai CH, Chu ML (1996) Tissue distribution and developmental expression of type XVI collagen in the mouse. Tissue Cell 28:155–164

    Article  CAS  PubMed  Google Scholar 

  • Lamande SR, Sigalas E, Pan TC, Chu ML, Dziadek M, Timpl R, Bateman JF (1998) The role of the alpha3(VI) chain in collagen VI assembly. Expression of an alpha3(VI) chain lacking N-terminal modules N10-N7 restores collagen VI assembly, secretion, and matrix deposition in an alpha3(VI)-deficient cell line. J Biol Chem 273:7423–7430

    Article  CAS  PubMed  Google Scholar 

  • Langan SM, Groves RW, West J (2011) The relationship between neurological disease and bullous pemphigoid: a population-based case-control study. J Invest Dermatol 131:631–636

    Article  CAS  PubMed  Google Scholar 

  • Latvanlehto A, Fox MA, Sormunen R, Tu H, Oikarainen T, Koski A, Naumenko N, Shakirzyanova A, Kallio M, Ilves M, Giniatullin R, Sanes JR, Pihlajaniemi T (2010) Muscle-derived collagen XIII regulates maturation of the skeletal neuromuscular junction. J Neurosci 30:12230–12241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leung AW, Wong SY, Chan D, Tam PP, Cheah KS (2010) Loss of procollagen IIA from the anterior mesendoderm disrupts the development of mouse embryonic forebrain. Dev Dyn 239:2319–2329

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Li J, Woo YM, Shen Z, Yao H, Cai Y, Lin MC, Poon WS (2017) Enhanced expression of Vastatin inhibits angiogenesis and prolongs survival in murine orthotopic glioblastoma model. BMC Cancer 17:126–128

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liao HM, Chao YL, Huang AL, Cheng MC, Chen YJ, Lee KF, Fang JS, Hsu CH, Chen CH (2012) Identification and characterization of three inherited genomic copy number variations associated with familial schizophrenia. Schizophr Res 139:229–236

    Article  PubMed  Google Scholar 

  • Logan CV, Cossins J, Rodriguez Cruz PM, Parry DA, Maxwell S, Martinez-Martinez P, Riepsaame J, Abdelhamed ZA, Lake AV, Moran M, Robb S, Chow G, Sewry C, Hopkins PM, Sheridan E, Jayawant S, Palace J, Johnson CA, Beeson D (2015) Congenital myasthenic syndrome type 19 is caused by mutations in COL13A1, encoding the atypical non-fibrillar collagen type XIII alpha1 chain. Am J Hum Genet 97:878–885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lui VC, Ng LJ, Nicholls J, Tam PP, Cheah KS (1995a) Tissue-specific and differential expression of alternatively spliced alpha 1(II) collagen mRNAs in early human embryos. Dev Dyn 203:198–211

    Article  CAS  PubMed  Google Scholar 

  • Lui VC, Kong RY, Nicholls J, Cheung AN, Cheah KS (1995b) The mRNAs for the three chains of human collagen type XI are widely distributed but not necessarily co-expressed: implications for homotrimeric, heterotrimeric and heterotypic collagen molecules. Biochem J 311(Pt 2):511–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahajan VB, Olney AH, Garrett P, Chary A, Dragan E, Lerner G, Murray J, Bassuk AG (2010) Collagen XVIII mutation in Knobloch syndrome with acute lymphoblastic leukemia. Am J Med Genet A 152A:2875–2879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mao M, Alavi MV, Labelle-Dumais C, Gould DB (2015) Type IV collagens and basement membrane diseases: cell biology and pathogenic mechanisms. Curr Top Membr 76:61–116

    Article  CAS  PubMed  Google Scholar 

  • Marazza G, Pham HC, Scharer L, Pedrazzetti PP, Hunziker T, Trueb RM, Hohl D, Itin P, Lautenschlager S, Naldi L, Borradori L, Autoimmune bullous disease Swiss study group (2009) Incidence of bullous pemphigoid and pemphigus in Switzerland: a 2-year prospective study. Br J Dermatol 161:861–868

    Article  CAS  PubMed  Google Scholar 

  • Marneros AG, Keene DR, Hansen U, Fukai N, Moulton K, Goletz PL, Moiseyev G, Pawlyk BS, Halfter W, Dong S, Shibata M, Li T, Crouch RK, Bruckner P, Olsen BR (2004) Collagen XVIII/endostatin is essential for vision and retinal pigment epithelial function. EMBO J 23:89–99

    Article  CAS  PubMed  Google Scholar 

  • Marquardt RJ, Li Y (2019) Congenital myasthenic syndrome type 19 due to a novel mutation in the COL13A1 GENE. Muscle Nerve 60:E3–E4

    PubMed  Google Scholar 

  • Matsuo N, Tanaka S, Yoshioka H, Koch M, Gordon MK, Ramirez F (2008) Collagen XXIV (Col24a1) gene expression is a specific marker of osteoblast differentiation and bone formation. Connect Tissue Res 49:68–75

    Article  CAS  PubMed  Google Scholar 

  • Maxwell WL, Duance VC, Lehto M, Ashurst DE, Berry M (1984) The distribution of types I, III, IV and V collagens in penetrant lesions of the central nervous system of the rat. Histochem J 16:1215–1229

    Article  CAS  PubMed  Google Scholar 

  • Meyer F, Moussian B (2009) Drosophila multiplexin (Dmp) modulates motor axon pathfinding accuracy. Develop Growth Differ 51:483–498

    Article  CAS  Google Scholar 

  • Miner JH, Sanes JR (1994) Collagen IV alpha 3, alpha 4, and alpha 5 chains in rodent basal laminae: sequence, distribution, association with laminins, and developmental switches. J Cell Biol 127:879–891

    Article  CAS  PubMed  Google Scholar 

  • Miosge N, Simniok T, Sprysch P, Herken R (2003) The collagen type XVIII endostatin domain is co-localized with perlecan in basement membranes in vivo. J Histochem Cytochem 51:285–296

    Article  CAS  PubMed  Google Scholar 

  • Miyake M, Hori S, Morizawa Y, Tatsumi Y, Toritsuka M, Ohnishi S, Shimada K, Furuya H, Khadka VS, Deng Y, Ohnishi K, Iida K, Gotoh D, Nakai Y, Inoue T, Anai S, Torimoto K, Aoki K, Tanaka N, Konishi N, Fujimoto K (2017) Collagen type IV alpha 1 (COL4A1) and collagen type XIII alpha 1 (COL13A1) produced in cancer cells promote tumor budding at the invasion front in human urothelial carcinoma of the bladder. Oncotarget 8:36099–36114

    Article  PubMed  PubMed Central  Google Scholar 

  • Mokarram N, Merchant A, Mukhatyar V, Patel G, Bellamkonda RV (2012) Effect of modulating macrophage phenotype on peripheral nerve repair. Biomaterials 33:8793–8801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monavarfeshani A, Knill CN, Sabbagh U, Su J, Fox MA (2017) Region- and cell-specific expression of transmembrane collagens in mouse brain. Front Integr Neurosci 11:20

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mouw JK, Ou G, Weaver VM (2014) Extracellular matrix assembly: a multiscale deconstruction. Nat Rev Mol Cell Biol 15:771–785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munezane H, Oizumi H, Wakabayashi T, Nishio S, Hirasawa T, Sato T, Harada A, Yoshida T, Eguchi T, Yamanashi Y, Hashimoto T, Iwatsubo T (2019) Roles of collagen XXV and its putative receptors PTPsigma/delta in intramuscular motor innervation and congenital cranial dysinnervation disorder. Cell Rep 29:4362–4376.e6

    Article  CAS  PubMed  Google Scholar 

  • Munji RN, Soung AL, Weiner GA, Sohet F, Semple BD, Trivedi A, Gimlin K, Kotoda M, Korai M, Aydin S, Batugal A, Cabangcala AC, Schupp PG, Oldham MC, Hashimoto T, Noble-Haeusslein LJ, Daneman R (2019) Profiling the mouse brain endothelial transcriptome in health and disease models reveals a core blood-brain barrier dysfunction module. Nat Neurosci 22:1892–1902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muona P, Jaakkola S, Zhang RZ, Pan TC, Pelliniemi L, Risteli L, Chu ML, Uitto J, Peltonen J (1993) Hyperglycemic glucose concentrations up-regulate the expression of type VI collagen in vitro. Relevance to alterations of peripheral nerves in diabetes mellitus. Am J Pathol 142:1586–1597

    CAS  PubMed  PubMed Central  Google Scholar 

  • Muona A, Eklund L, Väisänen T, Pihlajaniemi T (2002) Developmentally regulated expression of type XV collagen correlates with abnormalities in Col15a1(−/−) mice. Matrix Biol 21:89–102

    Article  CAS  PubMed  Google Scholar 

  • Murad S, Grove D, Lindberg KA, Reynolds G, Sivarajah A, Pinnell SR (1981) Regulation of collagen synthesis by ascorbic acid. Proc Natl Acad Sci USA 78:2879–2882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muragaki Y, Shiota C, Inoue M, Ooshima A, Olsen BR, Ninomiya Y (1992) alpha 1(VIII)-collagen gene transcripts encode a short-chain collagen polypeptide and are expressed by various epithelial, endothelial and mesenchymal cells in newborn mouse tissues. Eur J Biochem 207:895–902

    Article  CAS  PubMed  Google Scholar 

  • Myers JC, Li D, Bageris A, Abraham V, Dion AS, Amenta PS (1997) Biochemical and immunohistochemical characterization of human type XIX defines a novel class of basement membrane zone collagens. Am J Pathol 151:1729–1740

    CAS  PubMed  PubMed Central  Google Scholar 

  • Myers JC, Li D, Amenta PS, Clark CC, Nagaswami C, Weisel JW (2003) Type XIX collagen purified from human umbilical cord is characterized by multiple sharp kinks delineating collagenous subdomains and by intermolecular aggregates via globular, disulfide-linked, and heparin-binding amino termini. J Biol Chem 278:32047–32057

    Article  CAS  PubMed  Google Scholar 

  • Myllyharju J, Kivirikko KI (2004) Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20:33–43

    Article  CAS  PubMed  Google Scholar 

  • Nah HD, Barembaum M, Upholt WB (1992) The chicken alpha 1 (XI) collagen gene is widely expressed in embryonic tissues. J Biol Chem 267:22581–22586

    Article  CAS  PubMed  Google Scholar 

  • Nguyen QT, Sanes JR, Lichtman JW (2002) Pre-existing pathways promote precise projection patterns. Nat Neurosci 5:861–867

    Article  CAS  PubMed  Google Scholar 

  • Novak U, Kaye AH (2000) Extracellular matrix and the brain: components and function. J Clin Neurosci 7:280–290

    Article  CAS  PubMed  Google Scholar 

  • O’Brien RJ, Wong PC (2011) Amyloid precursor protein processing and Alzheimer’s disease. Annu Rev Neurosci 34:185–204

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oh SP, Griffith CM, Hay ED, Olsen BR (1993) Tissue-specific expression of type XII collagen during mouse embryonic development. Dev Dyn 196:37–46

    Article  CAS  PubMed  Google Scholar 

  • Oprisoreanu AM, Smith HL, Arya S, Webster R, Zhong Z, Wehner D, Cardozo MJ, Becker T, Talbot K, Becker CG (2019) Interaction of axonal chondrolectin with collagen XIXa1 is necessary for precise neuromuscular junction formation. Cell Rep 29:1082–1098.e10

    Article  CAS  PubMed  Google Scholar 

  • O’Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, Flynn E, Birkhead JR, Olsen BR, Folkman J (1997) Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 88:277–285

    Article  PubMed  Google Scholar 

  • Osada Y, Hashimoto T, Nishimura A, Matsuo Y, Wakabayashi T, Iwatsubo T (2005) CLAC binds to amyloid beta peptides through the positively charged amino acid cluster within the collagenous domain 1 and inhibits formation of amyloid fibrils. J Biol Chem 280:8596–8605

    Article  CAS  PubMed  Google Scholar 

  • Osawa T, Ide C (1986) Changes in thickness of collagen fibrils in the endo- and epineurium of the mouse sciatic nerve during development. Acta Anat (Basel) 125:245–251

    Article  CAS  Google Scholar 

  • Palumbo C, Massa R, Panico MB, Di Muzio A, Sinibaldi P, Bernardi G, Modesti A (2002) Peripheral nerve extracellular matrix remodeling in Charcot-Marie-Tooth type I disease. Acta Neuropathol 104:287–296

    Article  CAS  PubMed  Google Scholar 

  • Parker SR, Dyson S, Brisman S, Pennie M, Swerlick RA, Khan R, Manos S, Korman BD, Xia Z, Korman NJ (2008) Mortality of bullous pemphigoid: an evaluation of 223 patients and comparison with the mortality in the general population in the United States. J Am Acad Dermatol 59:582–588

    Article  PubMed  Google Scholar 

  • Passos-Bueno MR, Suzuki OT, Armelin-Correa LM, Sertie AL, Errera FI, Bagatini K, Kok F, Leite KR (2006) Mutations in collagen 18A1 and their relevance to the human phenotype. An Acad Bras Cienc 78:123–131

    Article  CAS  PubMed  Google Scholar 

  • Paulus W, Sage EH, Liszka U, Iruela-Arispe ML, Jellinger K (1991) Increased levels of type VIII collagen in human brain tumours compared to normal brain tissue and non-neoplastic cerebral disorders. Br J Cancer 63:367–371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paulus W, Baur I, Liszka U, Drlicek M, Leigh I, Bruckner-Tuderman L (1995) Expression of type VII collagen, the major anchoring fibril component, in normal and neoplastic human nervous system. Virchows Arch 426:199–202

    Article  CAS  PubMed  Google Scholar 

  • Peltonen J, Jaakkola S, Hsiao LL, Timpl R, Chu ML, Uitto J (1990) Type VI collagen. In situ hybridizations and immunohistochemistry reveal abundant mRNA and protein levels in human neurofibroma, schwannoma and normal peripheral nerve tissues. Lab Investig 62:487–492

    CAS  PubMed  Google Scholar 

  • Perrin FE, Lacroix S, Aviles-Trigueros M, David S (2005) Involvement of monocyte chemoattractant protein-1, macrophage inflammatory protein-1alpha and interleukin-1beta in Wallerian degeneration. Brain 128:854–866

    Google Scholar 

  • Pöschl E, Schlotzer-Schrehardt U, Brachvogel B, Saito K, Ninomiya Y, Mayer U (2004) Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development 131:1619–1628

    Article  PubMed  CAS  Google Scholar 

  • Qin J, Liang J, Ding M (2014) Perlecan antagonizes collagen IV and ADAMTS9/GON-1 in restricting the growth of presynaptic boutons. J Neurosci 34:10311–10324

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ramanoudjame L, Rocancourt C, Laine J, Klein A, Joassard L, Gartioux C, Fleury M, Lyphout L, Kabashi E, Ciura S, Cousin X, Allamand V (2015) Two novel COLVI long chains in zebrafish that are essential for muscle development. Hum Mol Genet 24:6624–6639

    Article  CAS  PubMed  Google Scholar 

  • Rasi K, Hurskainen M, Kallio M, Staven S, Sormunen R, Heape AM, Avila RL, Kirschner D, Muona A, Tolonen U, Tanila H, Huhtala P, Soininen R, Pihlajaniemi T (2010) Lack of collagen XV impairs peripheral nerve maturation and, when combined with laminin-411 deficiency, leads to basement membrane abnormalities and sensorimotor dysfunction. J Neurosci 30:14490–14501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren Z, Hsu DY, Brieva J, Silverberg NB, Langan SM, Silverberg JI (2017) Hospitalization, inpatient burden and comorbidities associated with bullous pemphigoid in the U.S.A. Br J Dermatol 176:87–99

    Article  CAS  PubMed  Google Scholar 

  • Ricard-Blum S (2011) The collagen family. Cold Spring Harb Perspect Biol 3:a004978

    Article  PubMed  PubMed Central  Google Scholar 

  • Ricard-Blum S, Ballut L (2011) Matricryptins derived from collagens and proteoglycans. Front Biosci (Landmark Ed) 16:674–697

    Article  CAS  Google Scholar 

  • Ring C, Lemmon V, Halfter W (1995) Two chondroitin sulfate proteoglycans differentially expressed in the developing chick visual system. Dev Biol 168:11–27

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez Cruz PM, Cossins J, Estephan EP, Munell F, Selby K, Hirano M, Maroofin R, Mehrjardi MYV, Chow G, Carr A, Manzur A, Robb S, Munot P, Wei Liu W, Banka S, Fraser H, De Goede C, Zanoteli E, Conti Reed U, Sage A, Gratacos M, Macaya A, Dusl M, Senderek J, Topf A, Hofer M, Knight R, Ramdas S, Jayawant S, Lochmuller H, Palace J, Beeson D (2019) The clinical spectrum of the congenital myasthenic syndrome resulting from COL13A1 mutations. Brain 142:1547–1560

    Article  PubMed  PubMed Central  Google Scholar 

  • Roggendorf W, Opitz H, Schuppan D (1988) Altered expression of collagen type VI in brain vessels of patients with chronic hypertension. A comparison with the distribution of collagen IV and procollagen III. Acta Neuropathol 77:55–60

    Article  CAS  PubMed  Google Scholar 

  • Rohrbough J, Rushton E, Woodruff E, Fergestad T, Vigneswaran K, Broadie K (2007) Presynaptic establishment of the synaptic cleft extracellular matrix is required for post-synaptic differentiation. Genes Dev 21:2607–2628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roulet M, Ruggiero F, Karsenty G, LeGuellec D (2007) A comprehensive study of the spatial and temporal expression of the col5a1 gene in mouse embryos: a clue for understanding collagen V function in developing connective tissues. Cell Tissue Res 327:323–332

    Article  CAS  PubMed  Google Scholar 

  • Saarela J, Rehn M, Oikarinen A, Autio-Harmainen H, Pihlajaniemi T (1998) The short and long forms of type XVIII collagen show clear tissue specificities in their expression and location in basement membrane zones in humans. Am J Pathol 153:611–626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sage H, Balian G, Vogel AM, Bornstein P (1984) Type VIII collagen. Synthesis by normal and malignant cells in culture. Lab Investig 50:219–231

    CAS  PubMed  Google Scholar 

  • Sajanti J, Björkstrand AS, Finnila S, Heikkinen E, Peltonen J, Majamaa K (1999) Increase of collagen synthesis and deposition in the arachnoid and the dura following subarachnoid hemorrhage in the rat. Biochim Biophys Acta 1454:209–216

    Article  CAS  PubMed  Google Scholar 

  • Salza R, Oudart JB, Ramont L, Maquart FX, Bakchine S, Thoannes H, Ricard-Blum S (2015) Endostatin level in cerebrospinal fluid of patients with Alzheimer’s disease. J Alzheimers Dis 44:1253–1261

    Article  CAS  PubMed  Google Scholar 

  • Sandberg M, Tamminen M, Hirvonen H, Vuorio E, Pihlajaniemi T (1989) Expression of mRNAs coding for the alpha 1 chain of type XIII collagen in human fetal tissues: comparison with expression of mRNAs for collagen types I, II, and III. J Cell Biol 109:1371–1379

    Article  CAS  PubMed  Google Scholar 

  • Sandberg MM, Hirvonen HE, Elima KJ, Vuorio EI (1993) Co-expression of collagens II and XI and alternative splicing of exon 2 of collagen II in several developing human tissues. Biochem J 294(Pt 2):595–602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandberg-Lall M, Hägg PO, Wahlström I, Pihlajaniemi T (2000) Type XIII collagen is widely expressed in the adult and developing human eye and accentuated in the ciliary muscle, the optic nerve and the neural retina. Exp Eye Res 70:401–410

    Article  CAS  PubMed  Google Scholar 

  • Sanes JR, Lichtman JW (1999) Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22:389–442

    Article  CAS  PubMed  Google Scholar 

  • Sanes JR, Lichtman JW (2001) Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci 2:791–805

    Article  CAS  PubMed  Google Scholar 

  • Schneider VA, Granato M (2006) The myotomal diwanka (lh3) glycosyltransferase and type XVIII collagen are critical for motor growth cone migration. Neuron 50:683–695

    Article  CAS  PubMed  Google Scholar 

  • Schnoor M, Cullen P, Lorkowski J, Stolle K, Robenek H, Troyer D, Rauterberg J, Lorkowski S (2008) Production of type VI collagen by human macrophages: a new dimension in macrophage functional heterogeneity. J Immunol 180:5707–5719

    Article  CAS  PubMed  Google Scholar 

  • Senner V, Ratzinger S, Mertsch S, Grassel S, Paulus W (2008) Collagen XVI expression is upregulated in glioblastomas and promotes tumor cell adhesion. FEBS Lett 582:3293–3300

    Article  CAS  PubMed  Google Scholar 

  • Seppänen A, Autio-Harmainen H, Alafuzoff I, Särkioja T, Veijola J, Hurskainen T, Bruckner-Tuderman L, Tasanen K, Majamaa K (2006) Collagen XVII is expressed in human CNS neurons. Matrix Biol 25:185–188

    Article  PubMed  CAS  Google Scholar 

  • Seppänen A, Suuronen T, Hofmann SC, Majamaa K, Alafuzoff I (2007) Distribution of collagen XVII in the human brain. Brain Res 1158:50–56

    Article  PubMed  CAS  Google Scholar 

  • Seppänen A, Pikkarainen M, Hartikainen P, Hofmann SC, Majamaa K, Alafuzoff I (2009) Expression of collagen XVII and ubiquitin-binding protein p62 in motor neuron disease. Brain Res 1247:171–177

    Article  PubMed  CAS  Google Scholar 

  • Seppänen A, Miettinen R, Alafuzoff I (2010) Neuronal collagen XVII is localized to lipofuscin granules. Neuroreport 21:1090–1094

    Article  PubMed  CAS  Google Scholar 

  • Seppinen L, Pihlajaniemi T (2011) The multiple functions of collagen XVIII in development and disease. Matrix Biol 30:83–92

    Article  CAS  PubMed  Google Scholar 

  • Sertie AL, Sossi V, Camargo AA, Zatz M, Brahe C, Passos-Bueno MR (2000) Collagen XVIII, containing an endogenous inhibitor of angiogenesis and tumor growth, plays a critical role in the maintenance of retinal structure and in neural tube closure (Knobloch syndrome). Hum Mol Genet 9:2051–2058

    Article  CAS  PubMed  Google Scholar 

  • Sharif Y, Jumah F, Coplan L, Krosser A, Sharif K, Tubbs RS (2018) Blood brain barrier: a review of its anatomy and physiology in health and disease. Clin Anat 31:812–823

    Article  PubMed  Google Scholar 

  • Shellswell GB, Restall DJ, Duance VC, Bailey AJ (1979) Identification and differential distribution of collagen types in the central and peripheral nervous systems. FEBS Lett 106:305–308

    Article  CAS  PubMed  Google Scholar 

  • Shinwari JM, Khan A, Awad S, Shinwari Z, Alaiya A, Alanazi M, Tahir A, Poizat C, Al Tassan N (2015) Recessive mutations in COL25A1 are a cause of congenital cranial dysinnervation disorder. Am J Hum Genet 96:147–152

    Google Scholar 

  • Sievers J, Pehlemann FW, Gude S, Berry M (1994) Meningeal cells organize the superficial glia limitans of the cerebellum and produce components of both the interstitial matrix and the basement membrane. J Neurocytol 23:135–149

    Article  CAS  PubMed  Google Scholar 

  • Söderberg L, Kakuyama H, Moller A, Ito A, Winblad B, Tjernberg LO, Naslund J (2005) Characterization of the Alzheimer’s disease-associated CLAC protein and identification of an amyloid beta-peptide-binding site. J Biol Chem 280:1007–1015

    Article  PubMed  CAS  Google Scholar 

  • Song I, Dityatev A (2018) Crosstalk between glia, extracellular matrix and neurons. Brain Res Bull 136:101–108

    Article  CAS  PubMed  Google Scholar 

  • Spivey KA, Banyard J, Solis LM, Wistuba II, Barletta JA, Gandhi L, Feldman HA, Rodig SJ, Chirieac LR, Zetter BR (2010) Collagen XXIII: a potential biomarker for the detection of primary and recurrent non-small cell lung cancer. Cancer Epidemiol Biomarkers Prev 19:1362–1372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su J, Gorse K, Ramirez F, Fox MA (2010) Collagen XIX is expressed by interneurons and contributes to the formation of hippocampal synapses. J Comp Neurol 518:229–253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su J, Stenbjorn RS, Gorse K, Su K, Hauser KF, Ricard-Blum S, Pihlajaniemi T, Fox MA (2012) Target-derived matricryptins organize cerebellar synapse formation through alpha3beta1 integrins. Cell Rep 2:223–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su J, Chen J, Lippold K, Monavarfeshani A, Carrillo GL, Jenkins R, Fox MA (2016) Collagen-derived matricryptins promote inhibitory nerve terminal formation in the developing neocortex. J Cell Biol 212:721–736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su J, Cole J, Fox MA (2017) Loss of interneuron-derived collagen XIX leads to a reduction in Perineuronal nets in the mammalian telencephalon. ASN Neuro 9:1759091416689020

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sumiyoshi H, Laub F, Yoshioka H, Ramirez F (2001) Embryonic expression of type XIX collagen is transient and confined to muscle cells. Dev Dyn 220:155–162

    Article  CAS  PubMed  Google Scholar 

  • Sumiyoshi H, Mor N, Lee SY, Doty S, Henderson S, Tanaka S, Yoshioka H, Rattan S, Ramirez F (2004) Esophageal muscle physiology and morphogenesis require assembly of a collagen XIX-rich basement membrane zone. J Cell Biol 166:591–600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sund M, Väisänen T, Kaukinen S, Ilves M, Tu H, Autio-Harmainen H, Rauvala H, Pihlajaniemi T (2001a) Distinct expression of type XIII collagen in neuronal structures and other tissues during mouse development. Matrix Biol 20:215–231

    Article  CAS  PubMed  Google Scholar 

  • Sund M, Ylönen R, Tuomisto A, Sormunen R, Tahkola J, Kvist AP, Kontusaari S, Autio-Harmainen H, Pihlajaniemi T (2001b) Abnormal adherence junctions in the heart and reduced angiogenesis in transgenic mice overexpressing mutant type XIII collagen. EMBO J 20:5153–5164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki OT, Sertie AL, Der Kaloustian VM, Kok F, Carpenter M, Murray J, Czeizel AE, Kliemann SE, Rosemberg S, Monteiro M, Olsen BR, Passos-Bueno MR (2002) Molecular analysis of collagen XVIII reveals novel mutations, presence of a third isoform, and possible genetic heterogeneity in Knobloch syndrome. Am J Hum Genet 71:1320–1329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki O, Kague E, Bagatini K, Tu H, Heljasvaara R, Carvalhaes L, Gava E, de Oliveira G, Godoi P, Oliva G, Kitten G, Pihlajaniemi T, Passos-Bueno MR (2009) Novel pathogenic mutations and skin biopsy analysis in Knobloch syndrome. Mol Vis 15:801–809

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka T, Wakabayashi T, Oizumi H, Nishio S, Sato T, Harada A, Fujii D, Matsuo Y, Hashimoto T, Iwatsubo T (2014) CLAC-P/collagen type XXV is required for the intramuscular innervation of motoneurons during neuromuscular development. J Neurosci 34:1370–1379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor J, Unsoeld T, Hutter H (2018) The transmembrane collagen COL-99 guides longitudinally extending axons in C. elegans. Mol Cell Neurosci 89:9–19

    Article  CAS  PubMed  Google Scholar 

  • Teixeira VB, Cabral R, Brites MM, Vieira R, Figueiredo A (2014) Bullous pemphigoid and comorbidities: a case-control study in Portuguese patients. An Bras Dermatol 89:274–278

    Article  PubMed  PubMed Central  Google Scholar 

  • Tong Y, Xu Y, Scearce-Levie K, Ptacek LJ, Fu YH (2010) COL25A1 triggers and promotes Alzheimer’s disease-like pathology in vivo. Neurogenetics 11:41–52

    Article  CAS  PubMed  Google Scholar 

  • Tu H, Huhtala P, Lee HM, Adams JC, Pihlajaniemi T (2015) Membrane-associated collagens with interrupted triple-helices (MACITs): evolution from a bilaterian common ancestor and functional conservation in C. elegans. BMC Evol Biol 15:281–283

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tu H, Pirskanen-Matell R, Heikkinen A, Oikarainen T, Risteli J, Pihlajaniemi T (2018) Autoimmune antibodies to collagen XIII in myasthenia gravis patients. Muscle Nerve 57:506–510

    Article  CAS  PubMed  Google Scholar 

  • Unsoeld T, Park JO, Hutter H (2013) Discoidin domain receptors guide axons along longitudinal tracts in C. elegans. Dev Biol 374:142–152

    Article  CAS  PubMed  Google Scholar 

  • Urabe N, Naito I, Saito K, Yonezawa T, Sado Y, Yoshioka H, Kusachi S, Tsuji T, Ohtsuka A, Taguchi T, Murakami T, Ninomiya Y (2002) Basement membrane type IV collagen molecules in the choroid plexus, pia mater and capillaries in the mouse brain. Arch Histol Cytol 65:133–143

    Article  CAS  PubMed  Google Scholar 

  • Utriainen A, Sormunen R, Kettunen M, Carvalhaes LS, Sajanti E, Eklund L, Kauppinen R, Kitten GT, Pihlajaniemi T (2004) Structurally altered basement membranes and hydrocephalus in a type XVIII collagen deficient mouse line. Hum Mol Genet 13:2089–2099

    Article  CAS  PubMed  Google Scholar 

  • van Horssen J, Wilhelmus MM, Heljasvaara R, Pihlajaniemi T, Wesseling P, de Waal RM, Verbeek MM (2002) Collagen XVIII: a novel heparan sulfate proteoglycan associated with vascular amyloid depositions and senile plaques in Alzheimer’s disease brains. Brain Pathol 12:456–462

    Article  PubMed  Google Scholar 

  • Veit G, Kobbe B, Keene DR, Paulsson M, Koch M, Wagener R (2006) Collagen XXVIII, a novel von Willebrand factor A domain-containing protein with many imperfections in the collagenous domain. J Biol Chem 281:3494–3504

    Article  CAS  PubMed  Google Scholar 

  • Vitale P, Braghetta P, Volpin D, Bonaldo P, Bressan GM (2001) Mechanisms of transcriptional activation of the col6a1 gene during Schwann cell differentiation. Mech Dev 102:145–156

    Article  CAS  PubMed  Google Scholar 

  • Vogel W, Gish GD, Alves F, Pawson T (1997) The discoidin domain receptor tyrosine kinases are activated by collagen. Mol Cell 1:13–23

    Article  CAS  PubMed  Google Scholar 

  • Volonghi I, Pezzini A, Del Zotto E, Giossi A, Costa P, Ferrari D, Padovani A (2010) Role of COL4A1 in basement-membrane integrity and cerebral small-vessel disease. The COL4A1 stroke syndrome. Curr Med Chem 17:1317–1324

    Article  CAS  PubMed  Google Scholar 

  • Wälchli C, Koch M, Chiquet M, Odermatt BF, Trueb B (1994) Tissue-specific expression of the fibril-associated collagens XII and XIV. J Cell Sci 107(Pt 2):669–681

    Article  PubMed  Google Scholar 

  • White RJ, Wang Y, Tang P, Montezuma SR (2017) Knobloch syndrome associated with Polymicrogyria and early onset of retinal detachment: two case reports. BMC Ophthalmol 17:214-z

    Article  Google Scholar 

  • Xu L, Nirwane A, Yao Y (2018) Basement membrane and blood-brain barrier. Stroke Vasc Neurol 4:78–82

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamada Y, Sakuma J, Takeuchi I, Yasukochi Y, Kato K, Oguri M, Fujimaki T, Horibe H, Muramatsu M, Sawabe M, Fujiwara Y, Taniguchi Y, Obuchi S, Kawai H, Shinkai S, Mori S, Arai T, Tanaka M (2017) Identification of six polymorphisms as novel susceptibility loci for ischemic or hemorrhagic stroke by exome-wide association studies. Int J Mol Med 39:1477–1491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan X, Zhang C, Liang T, Yang F, Wang H, Wu F, Wang W, Wang Z, Cheng W, Xu J, Jiang T, Chen J, Ding Y (2017) A PTEN-COL17A1 fusion gene and its novel regulatory role in collagen XVII expression and GBM malignance. Oncotarget 8:85794–85803

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang H, Jin L, Sun X (2019) A thirteengene set efficiently predicts the prognosis of glioblastoma. Mol Med Rep 19:1613–1621

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ylikärppä R, Eklund L, Sormunen R, Muona A, Fukai N, Olsen BR, Pihlajaniemi T (2003) Double knockout mice reveal a lack of major functional compensation between collagens XV and XVIII. Matrix Biol 22:443–448

    Article  PubMed  CAS  Google Scholar 

  • Yoshida T, Kato K, Yokoi K, Oguri M, Watanabe S, Metoki N, Yoshida H, Satoh K, Aoyagi Y, Nozawa Y, Yamada Y (2010) Association of genetic variants with hemorrhagic stroke in Japanese individuals. Int J Mol Med 25:649–656

    Article  CAS  PubMed  Google Scholar 

  • Yoshioka H, Iyama K, Inoguchi K, Khaleduzzaman M, Ninomiya Y, Ramirez F (1995) Developmental pattern of expression of the mouse alpha 1 (XI) collagen gene (Col11a1). Dev Dyn 204:41–47

    Article  CAS  PubMed  Google Scholar 

  • Yu Phuan CZ, Yew YW, Tey HL (2017) Bullous pemphigoid and antecedent neurological diseases: an association with dementia. Indian J Dermatol Venereol Leprol 83:457–461

    Article  PubMed  Google Scholar 

  • Zainul Z, Heikkinen A, Koivisto H, Rautalahti I, Kallio M, Lin S, Härönen H, Norman O, Rüegg MA, Tanila H, Pihlajaniemi T (2018) Collagen XIII is required for neuromuscular synapse regeneration and functional recovery after peripheral nerve injury. J Neurosci 38:4243–4258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zech M, Lam DD, Francescatto L, Schormair B, Salminen AV, Jochim A, Wieland T, Lichtner P, Peters A, Gieger C, Lochmuller H, Strom TM, Haslinger B, Katsanis N, Winkelmann J (2015) Recessive mutations in the alpha3 (VI) collagen gene COL6A3 cause early-onset isolated dystonia. Am J Hum Genet 96:883–893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang WW, Ma KC, Andersen O, Sourander P, Tollesson PO, Olsson Y (1994) The microvascular changes in cases of hereditary multi-infarct disease of the brain. Acta Neuropathol 87:317–324

    Article  CAS  PubMed  Google Scholar 

  • Zhang ZY, Zhang Z, Fauser U, Artelt M, Burnet M, Schluesener HJ (2007) Dexamethasone transiently attenuates up-regulation of endostatin/collagen XVIII following traumatic brain injury. Neuroscience 147:720–726

    Article  CAS  PubMed  Google Scholar 

  • Zhang LS, Li HB, Zeng J, Yang Y, Ding C (2018) Knobloch syndrome caused by homozygous frameshift mutation of the COL18A1 gene in a Chinese pedigree. Int J Ophthalmol 11:918–922

    PubMed  PubMed Central  Google Scholar 

  • Zimmermann DR, Dours-Zimmermann MT (2008) Extracellular matrix of the central nervous system: from neglect to challenge. Histochem Cell Biol 130:635–653

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Biochemistry and Molecular Medicine, Center for Cell-Matrix Research, University of Oulu, Oulu, Finland

    Anne Heikkinen & Taina Pihlajaniemi

  2. Biocenter Oulu, University of Oulu, Oulu, Finland

    Anne Heikkinen

  3. School of Neuroscience, Virginia Tech, Blacksburg, VA, USA

    Michael A. Fox

  4. Fralin Biomedical Research Institute, Virginia Tech Carilion, Roanoke, VA, USA

    Michael A. Fox

  5. Department of Biological Sciences, Virginia Tech, Blacksburg, VA, USA

    Michael A. Fox

  6. Department of Pediatrics, Virginia Tech Carilion School of Medicine, Roanoke, VA, USA

    Michael A. Fox

Authors
  1. Anne Heikkinen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael A. Fox
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Taina Pihlajaniemi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Taina Pihlajaniemi .

Editor information

Editors and Affiliations

  1. Institut de Génomique Fonctionnelle de Lyon, ENS de Lyon, UMR CNRS, Université Lyon 1, LYON CEDEX 07, France

    Florence Ruggiero

Rights and permissions

Reprints and permissions

Copyright information

© 2021 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Heikkinen, A., Fox, M.A., Pihlajaniemi, T. (2021). Collagens as New Players in Nervous System Diseases. In: Ruggiero, F. (eds) The Collagen Superfamily and Collagenopathies. Biology of Extracellular Matrix, vol 8. Springer, Cham. https://doi.org/10.1007/978-3-030-67592-9_8

Download citation

Publish with us

Policies and ethics

Search

Navigation