Abstract
Recent discoveries of skeletal dysplasias caused by mutations in COPII coat proteins responsible for a key checkpoint in the secretory pathway have renewed the interest of matrix biologists in procollagen trafficking. Osteogenesis imperfecta (OI) has long been considered a disorder related to malformations or malfunction of type I collagen and its procollagen precursor (type I collagenopathy). However, OI and chondrodysplasia features of patients with mutations in inner COPII coat proteins SEC24D and SEC23A have revealed that procollagen malformations and trafficking defects might cause similar pathology. The goal of this review is to bridge our knowledge of procollagen biosynthesis, secretory protein trafficking, degradative protein trafficking, and genetic defects in skeletal development, in order to understand the pathophysiology of these and related diseases. We argue that folding in the Endoplasmic Reticulum (ER), sorting by COPII-bound proteins at ER exit sites, transport by COPI carriers to Golgi, and autophagy of misfolded molecules are all intimately linked and crucial steps in procollagen homeostasis. Disruptions in these processes by mutations in key regulatory proteins underlie common collagenopathy-like skeletal pathologies in a wide variety of hereditary disorders ranging from OI to lysosomal storage diseases.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- ARC:
-
arthrogryposis renal dysfunction and cholestasis syndrome
- COP:
-
coat protein complex I
- COPII:
-
coat protein complex II
- ECM:
-
extracellular matrix
- EGAD:
-
endosome and Golgi-associated degradation
- ER:
-
endoplasmic reticulum
- ERAD:
-
ER-associated degradation
- ERES:
-
ER exit site
- ERGIC:
-
ER-Golgi intermediate compartment
- ISR:
-
integrated cell stress response
- MCDS:
-
metaphyseal chondrodysplasia type Schmid
- OI:
-
osteogenesis imperfecta
- TGN:
-
trans-Golgi network
- UPR:
-
unfolded protein response
References
Adams BM, Oster ME, Hebert DN (2019) Protein quality control in the endoplasmic reticulum. Protein J 38(3):317–329
Anand AA, Walter P (2020) Structural insights into ISRIB, a memory-enhancing inhibitor of the integrated stress response. FEBS J 287(2):239–245
Appenzeller-Herzog C, Hauri HP (2006) The ER-Golgi intermediate compartment (ERGIC): in search of its identity and function. J Cell Sci 119(Pt 11):2173–2183
Aridor M (2018) COPII gets in shape: lessons derived from morphological aspects of early secretion. Traffic 19(11):823–839
Arnold WV, Fertala A (2013) Skeletal diseases caused by mutations that affect collagen structure and function. Int J Biochem Cell Biol 45(8):1556–1567
Arseni L, Lombardi A, Orioli D (2018) From structure to phenotype: impact of collagen alterations on human health. Int J Mol Sci 19(5):1407
Balasubramanian M, Padidela R, Pollitt RC, Bishop NJ, Mughal MZ, Offiah AC et al (2018) P4HB recurrent missense mutation causing Cole-carpenter syndrome. J Med Genet 55(3):158–165
Banushi B, Forneris F, Straatman-Iwanowska A, Strange A, Lyne AM, Rogerson C et al (2016) Regulation of post-Golgi LH3 trafficking is essential for collagen homeostasis. Nat Commun 7:12111
Barile FA, Guzowski DE, Ripley C, Siddiqi ZA, Bienkowski RS (1990) Ammonium chloride inhibits basal degradation of newly synthesized collagen in human fetal lung fibroblasts. Arch Biochem Biophys 276(1):125–131
Barlowe C, Helenius A (2016) Cargo capture and bulk flow in the early secretory pathway. Annu Rev Cell Dev Biol 32:197–222
Bartolomeo R, Cinque L, De Leonibus C, Forrester A, Salzano AC, Monfregola J et al (2017) mTORC1 hyperactivation arrests bone growth in lysosomal storage disorders by suppressing autophagy. J Clin Invest 127(10):3717–3729
Bateman JF, Boot-Handford RP, Lamande SR (2009) Genetic diseases of connective tissues: cellular and extracellular effects of ECM mutations. Nat Rev Genet 10(3):173–183
Bateman JF, Sampurno L, Maurizi A, Lamande SR, Sims NA, Cheng TL et al (2019) Effect of rapamycin on bone mass and strength in the alpha2(I)-G610C mouse model of osteogenesis imperfecta. J Cell Mol Med 23(3):1735–1745
Berg RA, Schwartz ML, Crystal RG (1980) Regulation of the production of secretory proteins: intracellular degradation of newly synthesized “defective” collagen. Proc Natl Acad Sci U S A 77(8):4746–4750
Besio R, Chow CW, Tonelli F, Marini JC, Forlino A (2019a) Bone biology: insights from osteogenesis imperfecta and related rare fragility syndromes. FEBS J 286(15):3033–3056
Besio R, Garibaldi N, Leoni L, Cipolla L, Sabbioneda S, Biggiogera M et al (2019b) Cellular stress due to impairment of collagen prolyl hydroxylation complex is rescued by the chaperone 4-phenylbutyrate. Dis Model Mech 12(6):dmm038521
Bethune J, Wieland FT (2018) Assembly of COPI and COPII vesicular coat proteins on membranes. Annu Rev Biophys 47:63–83
Bexiga MG, Simpson JC (2013) Human diseases associated with form and function of the Golgi complex. Int J Mol Sci 14(9):18670–18681
Beznoussenko GV, Parashuraman S, Rizzo R, Polishchuk R, Martella O, Di Giandomenico D et al (2014) Transport of soluble proteins through the Golgi occurs by diffusion via continuities across cisternae. elife 3:e02009
Bienkowski RS, Cowan MJ, McDonald JA, Crystal RG (1978) Degradation of newly synthesized collagen. J Biol Chem 253(12):4356–4363
Boncompain G, Divoux S, Gareil N, de Forges H, Lescure A, Latreche L et al (2012) Synchronization of secretory protein traffic in populations of cells. Nat Methods 9(5):493–498
Bonfanti L, Mironov AA Jr, Martinez-Menarguez JA, Martella O, Fusella A, Baldassarre M et al (1998) Procollagen traverses the Golgi stack without leaving the lumen of cisternae: evidence for cisternal maturation. Cell 95(7):993–1003
Bonifacino JS, Glick BS (2004) The mechanisms of vesicle budding and fusion. Cell 116(2):153–166
Bonifacino JS, Neefjes J (2017) Moving and positioning the endolysosomal system. Curr Opin Cell Biol 47:1–8
Bornstein P, Sage H (1989) Regulation of collagen gene expression. Prog Nucleic Acid Res Mol Biol 37:67–106
Boyadjiev SA, Fromme JC, Ben J, Chong SS, Nauta C, Hur DJ et al (2006) Cranio-lenticulo-sutural dysplasia is caused by a SEC23A mutation leading to abnormal endoplasmic-reticulum-to-Golgi trafficking. Nat Genet 38(10):1192–1197
Brandizzi F, Barlowe C (2013) Organization of the ER-Golgi interface for membrane traffic control. Nat Rev Mol Cell Biol 14(6):382–392
Cai H, Reinisch K, Ferro-Novick S (2007) Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev Cell 12(5):671–682
Canty EG, Kadler KE (2005) Procollagen trafficking, processing and fibrillogenesis. J Cell Sci 118(Pt 7):1341–1353
Centonze FG, Farhan H (2019) Crosstalk of endoplasmic reticulum exit sites and cellular signaling. FEBS Lett 593(17):2280–2288
Chan D, Ho MS, Cheah KS (2001) Aberrant signal peptide cleavage of collagen X in Schmid metaphyseal chondrodysplasia. Implications for the molecular basis of the disease. J Biol Chem 276(11):7992–7997
Chino H, Mizushima N (2020) ER-Phagy: quality control and turnover of endoplasmic reticulum. Trends Cell Biol 30(5):384–398
Christiansen HE, Schwarze U, Pyott SM, AlSwaid A, Al Balwi M, Alrasheed S et al (2010) Homozygosity for a missense mutation in SERPINH1, which encodes the collagen chaperone protein HSP47, results in severe recessive osteogenesis imperfecta. Am J Hum Genet 86(3):389–398
Clark CC (1979) The distribution and initial characterization of oligosaccharide units on the COOH-terminal propeptide extensions of the pro-alpha 1 and pro-alpha 2 chains of type I procollagen. J Biol Chem 254(21):10798–10802
Clarke LA, Hollak CE (2015) The clinical spectrum and pathophysiology of skeletal complications in lysosomal storage disorders. Best Pract Res Clin Endocrinol Metab 29(2):219–235
Cui Y, Parashar S, Zahoor M, Needham PG, Mari M, Zhu M et al (2019) A COPII subunit acts with an autophagy receptor to target endoplasmic reticulum for degradation. Science 365(6448):53–60
Cutrona MB, Morgan NE, Simpson JC (2018) Heritable skeletal disorders arising from defects in processing and transport of type I Procollagen from the ER: perspectives on possible therapeutic approaches. In: UlloaAguirre A, Tao YX (eds) Targeting trafficking in drug development. Handbook of experimental pharmacology, vol 245. Springer, Berlin, pp 191–225
Daley E, Streeten EA, Sorkin JD, Kuznetsova N, Shapses SA, Carleton SM et al (2010) Variable bone fragility associated with an Amish COL1A2 variant and a knock-in mouse model. J Bone Miner Res 25(2):247–261
Dancourt J, Barlowe C (2010) Protein sorting receptors in the early secretory pathway. Annu Rev Biochem 79:777–802
Delevoye C, Marks MS, Raposo G (2019) Lysosome-related organelles as functional adaptations of the endolysosomal system. Curr Opin Cell Biol 59:147–158
Dell’Angelica EC, Bonifacino JS (2019) Coatopathies: genetic disorders of protein coats. Annu Rev Cell Dev Biol 35:131–168
Di Martino R, Sticco L, Luini A (2019) Regulation of cargo export and sorting at the trans-Golgi network. FEBS Lett 593(17):2306–2318
Engel J, Bachinger HP (2005) Structure, stability and folding of the collagen triple helix. In: Brinckmann J, Notbohm H, Muller PK (eds) Collagen: primer in structure, processing and assembly, Topics in current chemistry, vol 247. Springer, Heidelberg, pp 7–33
Eyre DR, Weis MA (2013) Bone collagen: new clues to its mineralization mechanism from recessive osteogenesis imperfecta. Calcif Tissue Int 93(4):338–347
Faini M, Beck R, Wieland FT, Briggs JA (2013) Vesicle coats: structure, function, and general principles of assembly. Trends Cell Biol 23(6):279–288
Ferreira CR, Xia ZJ, Clement A, Parry DA, Davids M, Taylan F et al (2018) A recurrent De novo heterozygous COG4 substitution leads to Saul-Wilson syndrome, disrupted vesicular trafficking, and altered proteoglycan glycosylation. Am J Hum Genet 103(4):553–567
Fitzgerald J, Lamande SR, Bateman JF (1999) Proteasomal degradation of unassembled mutant type I collagen pro-alpha1(I) chains. J Biol Chem 274(39):27392–27398
Forlino A, Marini JC (2016) Osteogenesis imperfecta. Lancet 387(10028):1657–1671
Forlino A, Cabral WA, Barnes AM, Marini JC (2011) New perspectives on osteogenesis imperfecta. Nat Rev Endocrinol 7(9):540–557
Forrester A, De Leonibus C, Grumati P, Fasana E, Piemontese M, Staiano L et al (2019) A selective ER-phagy exerts procollagen quality control via a Calnexin-FAM134B complex. EMBO J 38(2):e99847
Fregno I, Molinari M (2019) Proteasomal and lysosomal clearance of faulty secretory proteins: ER-associated degradation (ERAD) and ER-to-lysosome-associated degradation (ERLAD) pathways. Crit Rev Biochem Mol Biol 54(2):153–163
Fromme JC, Ravazzola M, Hamamoto S, Al-Balwi M, Eyaid W, Boyadjiev SA et al (2007) The genetic basis of a craniofacial disease provides insight into COPII coat assembly. Dev Cell 13(5):623–634
Fujii KK, Taga Y, Sakai T, Ito S, Hattori S, Nagata K et al (2019) Lowering the culture temperature corrects collagen abnormalities caused by HSP47 gene knockout. Sci Rep 9(1):17433
Galluzzi L, Baehrecke EH, Ballabio A, Boya P, Bravo-San Pedro JM, Cecconi F et al (2017) Molecular definitions of autophagy and related processes. EMBO J 36(13):1811–1836
Garbes L, Kim K, Riess A, Hoyer-Kuhn H, Beleggia F, Bevot A et al (2015) Mutations in SEC24D, encoding a component of the COPII machinery, cause a Syndromic form of Osteogenesis Imperfecta. Am J Hum Genet 96(3):432–439
Geva Y, Schuldiner M (2014) The back and forth of cargo exit from the endoplasmic reticulum. Curr Biol 24(3):R130–R136
Gioia R, Tonelli F, Ceppi I, Biggiogera M, Leikin S, Fisher S et al (2017) The chaperone activity of 4PBA ameliorates the skeletal phenotype of Chihuahua, a zebrafish model for dominant osteogenesis imperfecta. Hum Mol Genet 26(15):2897–2911
Gissen P, Tee L, Johnson CA, Genin E, Caliebe A, Chitayat D et al (2006) Clinical and molecular genetic features of ARC syndrome. Hum Genet 120(3):396–409
Gorur A, Yuan L, Kenny SJ, Baba S, Xu K, Schekman R (2017) COPII-coated membranes function as transport carriers of intracellular procollagen I. J Cell Biol 216(6):1745–1759
Gotkin MG, Ripley CR, Lamande SR, Bateman JF, Bienkowski RS (2004) Intracellular trafficking and degradation of unassociated proalpha2 chains of collagen type I. Exp Cell Res 296(2):307–316
Guillemyn B, Kayserili H, Demuynck L, Sips P, De Paepe A, Syx D et al (2019) A homozygous pathogenic missense variant broadens the phenotypic and mutational spectrum of CREB3L1-related osteogenesis imperfecta. Hum Mol Genet 28(11):1801–1809
Guo Y, Sirkis DW, Schekman R (2014) Protein sorting at the trans-Golgi network. Annu Rev Cell Dev Biol 30:169–206
Halperin D, Kadir R, Perez Y, Drabkin M, Yogev Y, Wormser O et al (2019) SEC31A mutation affects ER homeostasis, causing a neurological syndrome. J Med Genet 56(3):139–148
Hidvegi T, Ewing M, Hale P, Dippold C, Beckett C, Kemp C et al (2010) An autophagy-enhancing drug promotes degradation of mutant alpha1-antitrypsin Z and reduces hepatic fibrosis. Science 329(5988):229–232
Hsu VW, Yang JS (2009) Mechanisms of COPI vesicle formation. FEBS Lett 583(23):3758–3763
Hsu VW, Lee SY, Yang JS (2009) The evolving understanding of COPI vesicle formation. Nat Rev Mol Cell Biol 10(5):360–364
Hubner CA, Dikic I (2020) ER-phagy and human diseases. Cell Death Differ 27(3):833–842
Hulmes DJS (2019) Roles of the procollagen C-propeptides in health and disease. Essays Biochem 63:313–323
Hwang J, Qi L (2018) Quality control in the endoplasmic reticulum: crosstalk between ERAD and UPR pathways. Trends Biochem Sci 43(8):593–605
Ishida Y, Nagata K (2009) Autophagy eliminates a specific species of misfolded procollagen and plays a protective role in cell survival against ER stress. Autophagy 5(8):1217–1219
Ishida Y, Kubota H, Yamamoto A, Kitamura A, Bachinger HP, Nagata K (2006) Type I collagen in Hsp47-null cells is aggregated in endoplasmic reticulum and deficient in N-propeptide processing and fibrillogenesis. Mol Biol Cell 17(5):2346–2355
Ishida Y, Yamamoto A, Kitamura A, Lamande SR, Yoshimori T, Bateman JF et al (2009) Autophagic elimination of misfolded procollagen aggregates in the endoplasmic reticulum as a means of cell protection. Mol Biol Cell 20(11):2744–2754
Ishikawa Y, Bachinger HP (2013) A molecular ensemble in the rER for procollagen maturation. Biochim Biophys Acta 1833(11):2479–2491
Ishikawa Y, Ito S, Nagata K, Sakai LY, Bachinger HP (2016) Intracellular mechanisms of molecular recognition and sorting for transport of large extracellular matrix molecules. Proc Natl Acad Sci U S A 113(41):E6036–E6E44
Izumi K, Brett M, Nishi E, Drunat S, Tan ES, Fujiki K et al (2016) ARCN1 mutations cause a recognizable craniofacial syndrome due to COPI-mediated transport defects. Am J Hum Genet 99(2):451–459
Jacobsen CM, Barber LA, Ayturk UM, Roberts HJ, Deal LE, Schwartz MA et al (2014) Targeting the LRP5 pathway improves bone properties in a mouse model of osteogenesis imperfecta. J Bone Miner Res 29(10):2297–2306
Jin L, Pahuja KB, Wickliffe KE, Gorur A, Baumgartel C, Schekman R et al (2012) Ubiquitin-dependent regulation of COPII coat size and function. Nature 482(7386):495–500
Kadler KE, Hill A, Canty-Laird EG (2008) Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators. Curr Opin Cell Biol 20(5):495–501
Kaushik S, Cuervo AM (2018) The coming of age of chaperone-mediated autophagy. Nat Rev Mol Cell Biol 19(6):365–381
Keller RB, Tran TT, Pyott SM, Pepin MG, Savarirayan R, McGillivray G et al (2018) Monoallelic and biallelic CREB3L1 variant causes mild and severe osteogenesis imperfecta, respectively. Genet Med 20(4):411–419
Khaminets A, Heinrich T, Mari M, Grumati P, Huebner AK, Akutsu M et al (2015) Regulation of endoplasmic reticulum turnover by selective autophagy. Nature 522(7556):354–358
Khoriaty R, Hesketh GG, Bernard A, Weyand AC, Mellacheruvu D, Zhu G et al (2018) Functions of the COPII gene paralogs SEC23A and SEC23B are interchangeable in vivo. Proc Natl Acad Sci U S A 115(33):E7748–E7E57
Kim SD, Pahuja KB, Ravazzola M, Yoon J, Boyadjiev SA, Hammamoto S et al (2012) The [corrected] SEC23-SEC31 [corrected] interface plays critical role for export of procollagen from the endoplasmic reticulum. J Biol Chem 287(13):10134–10144
Kizilyaprak C, Stierhof YD, Humbel BM (2019) Volume microscopy in biology: FIB-SEM tomography. Tissue Cell 57:123–128
Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A et al (2016) Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 12(1):1–222
Ko MK, Kay EP (2004) PDI-mediated ER retention and proteasomal degradation of procollagen I in corneal endothelial cells. Exp Cell Res 295(1):25–35
Koide T, Nagata K (2005) Collagen biosynthesis. In: Brinckmann J, Notbohm H, Muller PK (eds) Collagen: primer in structure, processing and assembly, Topics in current chemistry-series, vol 247. Springer, Heidelberg, pp 85–114
Koide T, Nishikawa Y, Asada S, Yamazaki CM, Takahara Y, Homma DL et al (2006) Specific recognition of the collagen triple helix by chaperone HSP47. II. The HSP47-binding structural motif in collagens and related proteins. J Biol Chem 281(16):11177–11185
Kondo Y, Fu J, Wang H, Hoover C, McDaniel JM, Steet R et al (2018) Site-1 protease deficiency causes human skeletal dysplasia due to defective inter-organelle protein trafficking. JCI Insight 3(14):e121596
Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T et al (2004) The role of autophagy during the early neonatal starvation period. Nature 432(7020):1032–1036
Lamande SR, Bateman JF (1999) Procollagen folding and assembly: the role of endoplasmic reticulum enzymes and molecular chaperones. Semin Cell Dev Biol 10(5):455–464
Lamande SR, Chessler SD, Golub SB, Byers PH, Chan D, Cole WG et al (1995) Endoplasmic reticulum-mediated quality control of type I collagen production by cells from osteogenesis imperfecta patients with mutations in the pro alpha 1 (I) chain carboxyl-terminal propeptide which impair subunit assembly. J Biol Chem 270(15):8642–8649
Leblond CP (1989) Synthesis and secretion of collagen by cells of connective tissue, bone, and dentin. Anat Rec 224(2):123–138
Leikina E, Mertts MV, Kuznetsova N, Leikin S (2002) Type I collagen is thermally unstable at body temperature. Proc Natl Acad Sci U S A 99(3):1314–1318
Lekszas C, Foresti O, Raote I, Liedtke D, Konig EM, Nanda I et al (2020) Biallelic TANGO1 mutations cause a novel syndromal disease due to hampered cellular collagen secretion. elife 9:e51319
Lerner DW, McCoy D, Isabella AJ, Mahowald AP, Gerlach GF, Chaudhry TA et al (2013) A Rab10-dependent mechanism for polarized basement membrane secretion during organ morphogenesis. Dev Cell 24(2):159–168
Li WW, Li J, Bao JK (2012) Microautophagy: lesser-known self-eating. Cell Mol Life Sci 69(7):1125–1136
Lindert U, Cabral WA, Ausavarat S, Tongkobpetch S, Ludin K, Barnes AM et al (2016) MBTPS2 mutations cause defective regulated intramembrane proteolysis in X-linked osteogenesis imperfecta. Nat Commun 7:11920
Lippincott-Schwartz J (2001) The secretory membrane system studied in real-time. Robert Feulgen prize lecture, 2001. Histochem Cell Biol 116(2):97–107
Lippincott-Schwartz J, Roberts TH, Hirschberg K (2000) Secretory protein trafficking and organelle dynamics in living cells. Annu Rev Cell Dev Biol 16:557–589
Lu CL, Kim J (2020) Consequences of mutations in the genes of the ER export machinery COPII in vertebrates. Cell Stress Chaperones 25(2):199–209
Ma W, Goldberg E, Goldberg J (2017) ER retention is imposed by COPII protein sorting and attenuated by 4-phenylbutyrate. elife 6:e26624
Makareeva E, Leikin S (2007) Procollagen triple helix assembly: an unconventional chaperone-assisted folding paradigm. PLoS One 2(10):e1029
Makareeva E, Aviles NA, Leikin S (2011) Chaperoning osteogenesis: new protein-folding disease paradigms. Trends Cell Biol 21(3):168–176
Makareeva E, Sun G, Mirigian LS, Mertz EL, Vera JC, Espinoza NA et al (2018) Substitutions for arginine at position 780 in triple helical domain of the alpha1(I) chain alter folding of the type I procollagen molecule and cause osteogenesis imperfecta. PLoS One 13(7):e0200264
Makareeva E, Omari S, Roberts-Pilgrim AM, Gorrell L, Mertz E, Khoury B et al (2019) Therapeutic targeting of autophagy in Osteogenesis Imperfecta. J Bone Miner Res 32(Suppl 1):FRI-920. Available at https://www.asbmr.org//education/2019-abstracts
Malhotra V, Erlmann P (2015) The pathway of collagen secretion. Annu Rev Cell Dev Biol 31:109–124
Marini JC, Forlino A, Cabral WA, Barnes AM, San Antonio JD, Milgrom S et al (2007) Consortium for osteogenesis imperfecta mutations in the helical domain of type I collagen: regions rich in lethal mutations align with collagen binding sites for integrins and proteoglycans. Hum Mutat 28(3):209–221
Marini JC, Forlino A, Bachinger HP, Bishop NJ, Byers PH, Paepe A et al (2017) Osteogenesis imperfecta. Nat Rev Dis Primers 3:17052
McCaughey J, Stephens DJ (2018) COPII-dependent ER export in animal cells: adaptation and control for diverse cargo. Histochem Cell Biol 150(2):119–131
McCaughey J, Stevenson NL, Cross S, Stephens DJ (2019) ER-to-Golgi trafficking of procollagen in the absence of large carriers. J Cell Biol 218(3):929–948
Mercer TJ, Gubas A, Tooze SA (2018) A molecular perspective of mammalian autophagosome biogenesis. J Biol Chem 293(15):5386–5395
Mertz EL, Makareeva E, Mirigian LS, Koon KY, Perosky JE, Kozloff KM et al (2016) Makings of a brittle bone: unexpected lessons from a low protein diet study of a mouse OI model. Matrix Biol 52-54:29–42
Mi Y, Wang W, Lu J, Zhang C, Wang Y, Ying H et al (2018) Proteasome-mediated degradation of collagen III by cortisol in amnion fibroblasts. J Mol Endocrinol 60(2):45–54
Miles CA, Ghelashvili M (1999) Polymer-in-a-box mechanism for the thermal stabilization of collagen molecules in fibers. Biophys J 76(6):3243–3252
Mirigian LS, Makareeva E, Mertz EL, Omari S, Roberts-Pilgrim AM, Oestreich AK et al (2016) Osteoblast malfunction caused by cell stress response to Procollagen Misfolding in alpha2(I)-G610C mouse model of Osteogenesis Imperfecta. J Bone Miner Res 31(8):1608–1616
Mironov AA (2014) ER-Golgi transport could occur in the absence of COPII vesicles. Nat Rev Mol Cell Biol 15(3):1
Mironov AA, Beznoussenko GV (2012) The kiss-and-run model of intra-Golgi transport. Int J Mol Sci 13(6):6800–6819
Mironov AA, Mironov AA Jr, Beznoussenko GV, Trucco A, Lupetti P, Smith JD et al (2003) ER-to-Golgi carriers arise through direct en bloc protrusion and multistage maturation of specialized ER exit domains. Dev Cell 5(4):583–594
Mizushima N (2019) The ATG conjugation systems in autophagy. Curr Opin Cell Biol 63:1–10
Moosa S, Chung BHY, Tung JYL, Altmuller J, Thiele H, Nurnberg P et al (2016) Mutations in SEC24D cause autosomal recessive osteogenesis imperfecta. Clin Genet 89(4):517–519
Mortier GR, Cohn DH, Cormier-Daire V, Hall C, Krakow D, Mundlos S et al (2019) Nosology and classification of genetic skeletal disorders: 2019 revision. Am J Med Genet A 179(12):2393–2419
Mullan LA, Mularczyk EJ, Kung LH, Forouhan M, Wragg JM, Goodacre R et al (2017) Increased intracellular proteolysis reduces disease severity in an ER stress-associated dwarfism. J Clin Invest 127(10):3861–3865
Nabavi N, Pustylnik S, Harrison RE (2012) Rab GTPase mediated procollagen trafficking in ascorbic acid stimulated osteoblasts. PLoS One 7(9):e46265
Nagai N, Hosokawa M, Itohara S, Adachi E, Matsushita T, Hosokawa N et al (2000) Embryonic lethality of molecular chaperone hsp47 knockout mice is associated with defects in collagen biosynthesis. J Cell Biol 150(6):1499–1506
Nogueira C, Erlmann P, Villeneuve J, Santos AJ, Martinez-Alonso E, Martinez-Menarguez JA et al (2014) SLY1 and Syntaxin 18 specify a distinct pathway for procollagen VII export from the endoplasmic reticulum. elife 3:e02784
Oku M, Sakai Y (2018) Three distinct types of microautophagy based on membrane dynamics and molecular machineries. BioEssays 40(6):e1800008
Omari S, Makareeva E, Roberts-Pilgrim A, Mirigian L, Jarnik M, Ott C et al (2018) Noncanonical autophagy at ER exit sites regulates procollagen turnover. Proc Natl Acad Sci U S A 115(43):E10099–E1E108
Omari S, Makareeva E, Gorrell L, Jarnik M, Lippincott-Schwartz J, Leikin S (2020) Mechanisms of procollagen and HSP47 sorting during ER-to-Golgi trafficking. Matrix Biol 93:79–94
Pakdel M, von Blume J (2018) Exploring new routes for secretory protein export from the trans-Golgi network. Mol Biol Cell 29(3):235–240
Pantazopoulou A, Glick BS (2019) A kinetic view of membrane traffic pathways can transcend the classical view of Golgi compartments. Front Cell Dev Biol 7:153
Papandreou ME, Tavernarakis N (2017) Autophagy and the endo/exosomal pathways in health and disease. Biotechnol J 12(1):1600175
Presley JF, Cole NB, Schroer TA, Hirschberg K, Zaal KJ, Lippincott-Schwartz J (1997) ER-to-Golgi transport visualized in living cells. Nature 389(6646):81–85
Privalov PL (1982) Stability of proteins. Proteins which do not present a single cooperative system. Adv Protein Chem 35:1–104
Privalov PL, Tiktopulo EI, Tischenko VM (1979) Stability and mobility of the collagen structure. J Mol Biol 127(2):203–216
Qi L, Tsai B, Arvan P (2017) New insights into the physiological role of endoplasmic reticulum-associated degradation. Trends Cell Biol 27(6):430–440
Ramachandran U, Peterkofsky B (1997) Aberrant O-glycosylation in the collagenous domain of pro alpha2(I) procollagen subunits synthesized by chemically transformed hamster fibroblasts. Arch Biochem Biophys 342(1):29–37
Raote I, Malhotra V (2019) Protein transport by vesicles and tunnels. J Cell Biol 218(3):737–739
Raote I, Ortega-Bellido M, Santos AJ, Foresti O, Zhang C, Garcia-Parajo MF et al (2018) TANGO1 builds a machine for collagen export by recruiting and spatially organizing COPII, tethers and membranes. elife 7:e32723
Rauch F, Fahiminiya S, Majewski J, Carrot-Zhang J, Boudko S, Glorieux F et al (2015) Cole-carpenter syndrome is caused by a heterozygous missense mutation in P4HB. Am J Hum Genet 96(3):425–431
Rautou PE, Mansouri A, Lebrec D, Durand F, Valla D, Moreau R (2010) Autophagy in liver diseases. J Hepatol 53(6):1123–1134
Reynolds HM, Zhang L, Tran DT, Ten Hagen KG (2019) Tango1 coordinates the formation of endoplasmic reticulum/Golgi docking sites to mediate secretory granule formation. J Biol Chem 294(51):19498–19510
Ripley CR, Bienkowski RS (1997) Localization of procollagen I in the lysosome/endosome system of human fibroblasts. Exp Cell Res 236(1):147–154
Robinson ME, Rauch F (2019) Mendelian bone fragility disorders. Bone 126:11–17
Rossi V, Lee B, Marom R (2019) Osteogenesis imperfecta: advancements in genetics and treatment. Curr Opin Pediatr 31(6):708–715
Roth J, Zuber C (2017) Quality control of glycoprotein folding and ERAD: the role of N-glycan handling, EDEM1 and OS-9. Histochem Cell Biol 147(2):269–284
Ruggiano A, Foresti O, Carvalho P (2014) Quality control: ER-associated degradation: protein quality control and beyond. J Cell Biol 204(6):869–879
Sacher M, Shahrzad N, Kamel H, Milev MP (2019) TRAPPopathies: an emerging set of disorders linked to variations in the genes encoding transport protein particle (TRAPP)-associated proteins. Traffic 20(1):5–26
Sahl SJ, Hell SW, Jakobs S (2017) Fluorescence nanoscopy in cell biology. Nat Rev Mol Cell Biol 18(11):685–701
Saito K, Maeda M (2019) Not just a cargo receptor for large cargoes; an emerging role of TANGO1 as an organizer of ER exit sites. J Biochem 166(2):115–119
Saito K, Chen M, Bard F, Chen S, Zhou H, Woodley D et al (2009) TANGO1 facilitates cargo loading at endoplasmic reticulum exit sites. Cell 136(5):891–902
Santos AJ, Raote I, Scarpa M, Brouwers N, Malhotra V (2015) TANGO1 recruits ERGIC membranes to the endoplasmic reticulum for procollagen export. elife 4:e10982
Saraste J, Marie M (2018) Intermediate compartment (IC): from pre-Golgi vacuoles to a semi-autonomous membrane system. Histochem Cell Biol 150(5):407–430
Satoh M, Hirayoshi K, Yokota S, Hosokawa N, Nagata K (1996) Intracellular interaction of collagen-specific stress protein HSP47 with newly synthesized procollagen. J Cell Biol 133(2):469–483
Scales SJ, Pepperkok R, Kreis TE (1997) Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COPII and COPI. Cell 90(6):1137–1148
Scheiber A, Suzuki A, Enomoto-Iwamoto M, Iwamoto M, Leikin S, Otsuru S (2019) 4-phenylbutyrate (4PBA) ameliorates growth deficiency in G610C mouse model of Osteogenesis Imperfecta. J Bone Miner Res 32(Suppl 1):1135. Available at https://www.asbmr.org//education/2019-abstracts
Schmidt O, Weyer Y, Baumann V, Widerin MA, Eising S, Angelova M et al (2019) Endosome and Golgi-associated degradation (EGAD) of membrane proteins regulates sphingolipid metabolism. EMBO J 38(15):e101433
Schwarze U, Cundy T, Liu YJ, Hofman PL, Byers PH (2019) Compound heterozygosity for a frameshift mutation and an upstream deletion that reduces expression of SERPINH1 in siblings with a moderate form of osteogenesis imperfecta. Am J Med Genet A 179(8):1466–1475
Shoulders MD, Raines RT (2009) Collagen structure and stability. Annu Rev Biochem 78:929–958
Smith T, Ferreira LR, Hebert C, Norris K, Sauk JJ (1995) Hsp47 and cyclophilin B traverse the endoplasmic reticulum with procollagen into pre-Golgi intermediate vesicles. A role for Hsp47 and cyclophilin B in the export of procollagen from the endoplasmic reticulum. J Biol Chem 270(31):18323–18328
Sprangers J, Rabouille C (2015) SEC16 in COPII coat dynamics at ER exit sites. Biochem Soc Trans 43(1):97–103
Subramanian A, Capalbo A, Iyengar NR, Rizzo R, di Campli A, Di Martino R et al (2019) Auto-regulation of secretory flux by sensing and responding to the folded cargo protein load in the endoplasmic reticulum. Cell 176(6):1461–1476
Tekirdag K, Cuervo AM (2018) Chaperone-mediated autophagy and endosomal microautophagy: joint by a chaperone. J Biol Chem 293(15):5414–5424
Thakker-Varia S, Anderson DW, Kuivaniemi H, Tromp G, Shin HG, van der Rest M et al (1995) Aberrant splicing of the type III procollagen mRNA leads to intracellular degradation of the protein in a patient with Ehlers-Danlos type IV. Hum Mutat 6(2):116–125
Townley AK, Feng Y, Schmidt K, Carter DA, Porter R, Verkade P et al (2008) Efficient coupling of Sec23-Sec24 to Sec13-Sec31 drives COPII-dependent collagen secretion and is essential for normal craniofacial development. J Cell Sci 121(Pt 18):3025–3034
Trelstad RL, Hayashi K (1979) Tendon collagen fibrillogenesis: intracellular subassemblies and cell surface changes associated with fibril growth. Dev Biol 71(2):228–242
Unlu G, Qi X, Gamazon ER, Melville DB, Patel N, Rushing AR et al (2020) Phenome-based approach identifies RIC1-linked Mendelian syndrome through zebrafish models, biobank associations and clinical studies. Nat Med 26(1):98–109
Vakifahmetoglu-Norberg H, Xia HG, Yuan J (2015) Pharmacologic agents targeting autophagy. J Clin Invest 125(1):5–13
Vanakker O, Callewaert B, Malfait F, Coucke P (2015) The genetics of soft connective tissue disorders. In: Chakravarti A, Green E (eds) Annual review of genomics and human genetics, vol 16, pp 229–255
Venditti R, Wilson C, De Matteis MA (2014) Exiting the ER: what we know and what we don’t. Trends Cell Biol 24(1):9–18
Wang C, Tan Z, Niu B, Tsang KY, Tai A, Chan WCW et al (2018) Inhibiting the integrated stress response pathway prevents aberrant chondrocyte differentiation thereby alleviating chondrodysplasia. elife 7:e37673
Weigel A, Chang C, Shtengel G, Hoffman D, Freeman M, Xu CS et al (2019) COPI and COPII cooperate at ER exit sites to support ER-to-Golgi protein trafficking revealed by 3D ultrastructure analyses and live-cell imaging. Mol Biol Cell M42:30. (abstract#)
Wirth M, Zhang W, Razi M, Nyoni L, Joshi D, O'Reilly N et al (2019) Molecular determinants regulating selective binding of autophagy adapters and receptors to ATG8 proteins. Nat Commun 10(1):2055
Yin X, Zhou C, Li J, Liu R, Shi B, Yuan Q et al (2019) Autophagy in bone homeostasis and the onset of osteoporosis. Bone Res 7:28
Yoshii SR, Kuma A, Akashi T, Hara T, Yamamoto A, Kurikawa Y et al (2016) Systemic analysis of Atg5-null mice rescued from neonatal lethality by transgenic ATG5 expression in neurons. Dev Cell 39(1):116–130
Yu L, Chen Y, Tooze SA (2018) Autophagy pathway: cellular and molecular mechanisms. Autophagy 14(2):207–215
Yuan L, Kenny SJ, Hemmati J, Xu K, Schekman R (2018) TANGO1 and SEC12 are copackaged with procollagen I to facilitate the generation of large COPII carriers. Proc Natl Acad Sci U S A 115(52):E12255–E12E64
Zamurs LK, Idoate MA, Hanssen E, Gomez-Ibanez A, Pastor P, Lamande SR (2015) Aberrant mitochondria in a Bethlem myopathy patient with a homozygous amino acid substitution that destabilizes the collagen VI alpha2(VI) chain. J Biol Chem 290(7):4272–4281
Zanetti G, Pahuja KB, Studer S, Shim S, Schekman R (2011) COPII and the regulation of protein sorting in mammals. Nat Cell Biol 14(1):20–28
Zhang H, Yue H, Wang C, Gu J, He J, Fu W et al (2017) Novel mutations in the SEC24D gene in Chinese families with autosomal recessive osteogenesis imperfecta. Osteoporos Int 28(4):1473–1480
Zou Y, Donkervoort S, Salo AM, Foley AR, Barnes AM, Hu Y et al (2017) P4HA1 mutations cause a unique congenital disorder of connective tissue involving tendon, bone, muscle and the eye. Hum Mol Genet 26(12):2207–2217
Acknowledgments
This work was supported by funding from the Intramural Research Program of NICHD, NIH.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Omari, S., Makareeva, E., Leikin, S. (2021). Procollagen Trafficking and its Implications in Osteogenesis Imperfecta. 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_2
Download citation
DOI: https://doi.org/10.1007/978-3-030-67592-9_2
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-67591-2
Online ISBN: 978-3-030-67592-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)