Abstract
Organ transplantation is currently the best strategy for treating end stage renal disease (ESRD) but the numbers of donor kidneys available are not sufficient to meet the needs of the ever-increasing ESRD population. Therefore, developments in the field of tissue engineering are necessary to provide alternative treatments. Decellularization and three-dimensional (3D) bioprinting strategies may serve as attractive novel options. Since successful tissue engineering requires an in -depth understanding of organ development and regulatory pathways, we discuss signaling in renal development and the composition of the renal extracellular matrix before presenting progress in the decellularization and 3D bioprinting fields.
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Adams JC, Watt FM (1993) Regulation of development and differentiation by the extracellular matrix. Development 117:1183–1198
Aldahmesh MA, Khan AO, Mohamed JY, Alkuraya H, Ahmed H, Bobis S, Al-Mesfer S, Alkuraya FS (2011) Identification of ADAMTS18 as a gene mutated in Knobloch syndrome. J Med Genet 48:597–601
Allen BL, Filla MS, Rapraeger AC (2001) Role of heparan sulfate as a tissue-specific regulator of FGF-4 and FGF receptor recognition. J Cell Biol 155:845–858
Aumailley M (2013) The laminin family. Cell Adhes Migr 7:48–55
Bagherie-Lachidan M, Reginensi A, Pan Q, Zaveri HP, Scott DA, Blencowe BJ, Helmbacher F, McNeill H (2015) Stromal Fat4 acts non-autonomously with Dchs1/2 to restrict the nephron progenitor pool. Development 142:2564–2573
Baratz KH, Tosakulwong N, Ryu E, Brown WL, Branham K, Chen W, Tran KD, Schmid-Kubista KE, Heckenlively JR, Swaroop A, Abecasis G, Bailey KR, Edwards AO (2010) E2-2 protein and Fuchs’s corneal dystrophy. N Engl J Med 363:1016–1024
Bielesz B, Sirin Y, Si H, Niranjan T, Gruenwald A, Ahn S, Kato H, Pullman J, Gessler M, Haase VH, Susztak K (2010) Epithelial Notch signaling regulates interstitial fibrosis development in the kidneys of mice and humans. J Clin Invest 120:4040–4054
Blank U, Brown A, Adams DC, Karolak MJ, Oxburgh L (2009) BMP7 promotes proliferation of nephron progenitor cells via a JNK-dependent mechanism. Development 136:3557–3566
Bolland F, Korossis S, Wilshaw SP, Ingham E, Fisher J, Kearney JN, Southgate J (2007) Development and characterisation of a full-thickness acellular porcine bladder matrix for tissue engineering. Biomaterials 28:1061–1070
Bonadio JF, Sage H, Cheng F, Bernstein J, Striker GE (1984) Localization of collagen types IV and V, laminin, and heparan sulfate proteoglycan to the basal lamina of kidney epithelial cells in transfilter metanephric culture. Am J Pathol 116:289–296
Borza CM, Su Y, Chen X, Yu L, Mont S, Chetyrkin S, Voziyan P, Hudson BG, Billings PC, Jo H, Bennett JS, Degrado WF, Eckes B, Zent R, Pozzi A (2012) Inhibition of integrin alpha2beta1 ameliorates glomerular injury. J Am Soc Nephrol 23:1027–1038
Boucaut JC, Darribere T, Boulekbache H, Thiery JP (1984) Prevention of gastrulation but not neurulation by antibodies to fibronectin in amphibian embryos. Nature 307:364–367
Brandenberger R, Schmidt A, Linton J, Wang D, Backus C, Denda S, Muller U, Reichardt LF (2001) Identification and characterization of a novel extracellular matrix protein nephronectin that is associated with integrin alpha8beta1 in the embryonic kidney. J Cell Biol 154:447–458
Brown AC, Muthukrishnan SD, Guay JA, Adams DC, Schafer DA, Fetting JL, Oxburgh L (2013) Role for compartmentalization in nephron progenitor differentiation. Proc Natl Acad Sci U S A 110:4640–4645
Brzoska HL, d’Esposito AM, Kolatsi-Joannou M, Patel V, Igarashi P, Lei Y, Finnell RH, Lythgoe MF, Woolf AS, Papakrivopoulou E, Long DA (2016) Planar cell polarity genes Celsr1 and Vangl2 are necessary for kidney growth, differentiation, and rostrocaudal patterning. Kidney Int 90:1274–1284
Byers PH, Duvic M, Atkinson M, Robinow M, Smith LT, Krane SM, Greally MT, Ludman M, Matalon R, Pauker S, Quanbeck D, Schwarze U (1997) Ehlers-Danlos syndrome type VIIA and VIIB result from splice-junction mutations or genomic deletions that involve exon 6 in the COL1A1 and COL1A2 genes of type I collagen. Am J Med Genet 72:94–105
Caralt M, Uzarski JS, Iacob S, Obergfell KP, Berg N, Bijonowski BM, Kiefer KM, Ward HH, Wandinger-Ness A, Miller WM, Zhang ZJ, Abecassis MM, Wertheim JA (2015) Optimization and critical evaluation of decellularization strategies to develop renal extracellular matrix scaffolds as biological templates for organ engineering and transplantation. Am J Transplant 15:64–75
Carroll TJ, Park JS, Hayashi S, Majumdar A, McMahon AP (2005) Wnt9b plays a central role in the regulation of mesenchymal to epithelial transitions underlying organogenesis of the mammalian urogenital system. Dev Cell 9:283–292
Castelletti F, Donadelli R, Banterla F, Hildebrandt F, Zipfel PF, Bresin E, Otto E, Skerka C, Renieri A, Todeschini M, Caprioli J, Caruso RM, Artuso R, Remuzzi G, Noris M (2008) Mutations in FN1 cause glomerulopathy with fibronectin deposits. Proc Natl Acad Sci U S A 105:2538–2543
Chen X, Moeckel G, Morrow JD, Cosgrove D, Harris RC, Fogo AB, Zent R, Pozzi A (2004) Lack of integrin alpha1beta1 leads to severe glomerulosclerosis after glomerular injury. Am J Pathol 165:617–630
Cheng HT, Kopan R (2005) The role of Notch signaling in specification of podocyte and proximal tubules within the developing mouse kidney. Kidney Int 68:1951–1952
Cheng HT, Miner JH, Lin M, Tansey MG, Roth K, Kopan R (2003) Gamma-secretase activity is dispensable for mesenchyme-to-epithelium transition but required for podocyte and proximal tubule formation in developing mouse kidney. Development 130:5031–5042
Cheng HT, Kim M, Valerius MT, Surendran K, Schuster-Gossler K, Gossler A, McMahon AP, Kopan R (2007) Notch2, but not Notch1, is required for proximal fate acquisition in the mammalian nephron. Development 134:801–811
Christiano AM, D’Alessio M, Paradisi M, Angelo C, Mazzanti C, Puddu P, Uitto J (1996) A common insertion mutation in COL7A1 in two Italian families with recessive dystrophic epidermolysis bullosa.J Invest Dermatol 106:679–684
Cosgrove D, Meehan DT, Grunkemeyer JA, Kornak JM, Sayers R, Hunter WJ, Samuelson GC (1996) Collagen COL4A3 knockout: a mouse model for autosomal Alport syndrome. Genes Dev 10:2981–2992
Costa-Barbosa FA, Balasubramanian R, Keefe KW, Shaw ND, Al-Tassan N, Plummer L, Dwyer AA, Buck CL, Choi JH, Seminara SB, Quinton R, Monies D, Meyer B, Hall JE, Pitteloud N, Crowley WF Jr (2013) Prioritizing genetic testing in patients with Kallmann syndrome using clinical phenotypes. J Clin Endocrinol Metab 98:E943–E953
Crapo PM, Gilbert TW, Badylak SF (2011) An overview of tissue and whole organ decellularization processes. Biomaterials 32:3233–3243
Cui X, Boland T (2009) Human microvasculature fabrication using thermal inkjet printing technology. Biomaterials 30:6221–6227
Cui X, Breitenkamp K, Lotz M, D’Lima D (2012) Synergistic action of fibroblast growth factor-2 and transforming growth factor-beta1 enhances bioprinted human neocartilage formation. Biotechnol Bioeng 109:2357–2368
Das A, Tanigawa S, Karner CM, Xin M, Lum L, Chen C, Olson EN, Perantoni AO, Carroll TJ (2013) Stromal-epithelial crosstalk regulates kidney progenitor cell differentiation. Nat Cell Biol 15:1035–1044
Davies J, Lyon M, Gallagher J, Garrod D (1995) Sulphated proteoglycan is required for collecting duct growth and branching but not nephron formation during kidney development. Development 121:1507–1517
Deshmukh SN, Dive AM, Moharil R, Munde P (2016) Enigmatic insight into collagen. J Oral Maxillofac Pathol 20:276–283
Devenport D (2014) The cell biology of planar cell polarity. J Cell Biol 207:171–179
Dudley AT, Godin RE, Robertson EJ (1999) Interaction between FGF and BMP signaling pathways regulates development of metanephric mesenchyme. Genes Dev 13:1601–1613
Ekblom P, Alitalo K, Vaheri A, Timpl R, Saxen L (1980) Induction of a basement membrane glycoprotein in embryonic kidney: possible role of laminin in morphogenesis. Proc Natl Acad Sci U S A 77:485–489
Ekblom P, Lehtonen E, Saxen L, Timpl R (1981) Shift in collagen type as an early response to induction of the metanephric mesenchyme. J Cell Biol 89:276–283
Ekblom P, Ekblom M, Fecker L, Klein G, Zhang HY, Kadoya Y, Chu ML, Mayer U, Timpl R (1994) Role of mesenchymal nidogen for epithelial morphogenesis in vitro. Development 120:2003–2014
Eyrich D, Brandl F, Appel B, Wiese H, Maier G, Wenzel M, Staudenmaier R, Goepferich A, Blunk T (2007) Long-term stable fibrin gels for cartilage engineering. Biomaterials 28:55–65
Faivre L, Le Merrer M, Douvier S, Laurent N, Thauvin-Robinet C, Rousseau T, Vereecke I, Sagot P, Delezoide AL, Coucke P, Mortier G (2004) Recurrence of achondrogenesis type II within the same family: evidence for germline mosaicism. Am J Med Genet A 126A:308–312
Fassihi H, Diba VC, Wessagowit V, Dopping-Hepenstal PJ, Jones CA, Burrows NP, McGrath JA (2005) Transient bullous dermolysis of the newborn in three generations. Br J Dermatol 153:1058–1063
Fetting JL, Guay JA, Karolak MJ, Iozzo RV, Adams DC, Maridas DE, Brown AC, Oxburgh L (2014) FOXD1 promotes nephron progenitor differentiation by repressing decorin in the embryonic kidney. Development 141:17–27
Geckil H, Xu F, Zhang X, Moon S, Demirci U (2010) Engineering hydrogels as extracellular matrix mimics. Nanomedicine (Lond) 5:469–484
George EL, Georges-Labouesse EN, Patel-King RS, Rayburn H, Hynes RO (1993) Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119:1079–1091
Georges-Labouesse E, Messaddeq N, Yehia G, Cadalbert L, Dierich A, Le Meur M (1996) Absence of integrin alpha 6 leads to epidermolysis bullosa and neonatal death in mice. Nat Genet 13:370–373
Germain DP, Herrera-Guzman Y (2004) Vascular Ehlers-Danlos syndrome. Ann Genet 47:1–9
Girgert R, Martin M, Kruegel J, Miosge N, Temme J, Eckes B, Müller GA, Gross O(2010) Integrin α2-deficient mice provide insights into specific functions of collagen receptors in the kidney.Fibrogenesis Tissue Repair 3:19
Gonzaga-Jauregui C, Gamble CN, Yuan B, Penney S, Jhangiani S, Muzny DM, Gibbs RA, Lupski JR, Hecht JT (2015) Mutations in COL27A1 cause steel syndrome and suggest a founder mutation effect in the Puerto Rican population. Eur J Hum Genet 23:342–346
Gottsch JD, Sundin OH, Liu SH, Jun AS, Broman KW, Stark WJ, Vito EC, Narang AK, Thompson JM, Magovern M (2005) Inheritance of a novel COL8A2 mutation defines a distinct early-onset subtype of Fuchs corneal dystrophy. Invest Ophthalmol Vis Sci 46:1934–1939
Grieshammer U, Cebrian C, Ilagan R, Meyers E, Herzlinger D, Martin GR (2005) FGF8 is required for cell survival at distinct stages of nephrogenesis and for regulation of gene expression in nascent nephrons. Development 132:3847–3857
Guillotin B, Souquet A, Catros S, Duocastella M, Pippenger B, Bellance S, Bareille R, Remy M, Bordenave L, Amedee J, Guillemot F (2010) Laser assisted bioprinting of engineered tissue with high cell density and microscale organization. Biomaterials 31:7250–7256
Halt K, Vainio S (2014) Coordination of kidney organogenesis by Wnt signaling. Pediatr Nephrol 29:737–744
Harel T, Rabinowitz R, Hendler N, Galil A, Flusser H, Chemke J, Gradstein L, Lifshitz T, Ofir R, Elbedour K, Birk OS (2005) COL11A2 mutation associated with autosomal recessive Weissenbacher-Zweymuller syndrome: molecular and clinical overlap with otospondylomegaepiphyseal dysplasia (OSMED). Am J Med Genet A 132A:33–35
Hartner A, Schocklmann H, Prols F, Muller U, Sterzel RB (1999) Alpha8 integrin in glomerular mesangial cells and in experimental glomerulonephritis. Kidney Int 56:1468–1480
Has C, Sparta G, Kiritsi D, Weibel L, Moeller A, Vega-Warner V, Waters A, He Y, Anikster Y, Esser P, Straub BK, Hausser I, Bockenhauer D, Dekel B, Hildebrandt F, Bruckner-Tuderman L, Laube GF (2012) Integrin alpha3 mutations with kidney, lung, and skin disease. N Engl J Med 366:1508–1514
Hesuani Y, Pereira FDAS, Parfenov V, Koudan E, Mitryashkin A, Replyanski N, Kasyanov V, Knyazeva A, Bulanova E, Mironov V (2016) Design and implementation of novel multifunctional 3D Bioprinter. 3D Print Addit Manuf 3:64
Higashiyama S, Abraham JA, Klagsbrun M (1993) Heparin-binding EGF-like growth factor stimulation of smooth muscle cell migration: dependence on interactions with cell surface heparan sulfate. J Cell Biol 122:933–940
Hildebrand A, Romaris M, Rasmussen LM, Heinegard D, Twardzik DR, Border WA, Ruoslahti E (1994) Interaction of the small interstitial proteoglycans biglycan, decorin and fibromodulin with transforming growth factor beta. Biochem J 302:527–534
Hsu HH, Murasawa Y, Qi P, Nishimura Y, Wang PC (2013) Type V collagen fibrils in mouse metanephroi. Biochem Biophys Res Commun 441:649–654
Hu C, Sun L, Xiao L, Han Y, Fu X, Xiong X, Xu X, Liu Y, Yang S, Liu F, Kanwar YS (2015) Insights into the mechanisms involved in the expression and regulation of extracellular matrix proteins in diabetic nephropathy. Curr Med Chem 22:2858–2870
Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110:673–687
Ignotz RA, Massague J (1986) Transforming growth factor-beta stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. J Biol Chem 261:4337–4345
Ikegawa S, Nishimura G, Nagai T, Hasegawa T, Ohashi H, Nakamura Y (1998) Mutation of the type X collagen gene (COL10A1) causes spondylometaphyseal dysplasia. Am J Hum Genet 63:1659–1662
Jalali M, Nikravesh MR, Moeen AA, Karimfar MH, Saidinejat S, Mohammadi S, Rafighdoost H (2009) Inductive role of collagen type IV during nephrogenesis in mice. Urol J 6:289–294
Jefferson JA, Lemmink HH, Hughes AE, Hill CM, Smeets HJ, Doherty CC, Maxwell AP (1997) Autosomal dominant Alport syndrome linked to the type IV collage alpha 3 and alpha 4 genes (COL4A3 and COL4A4). Nephrol Dial Transplant 12:1595–1599
Kagami S, Border WA, Miller DE, Noble NA (1994) Angiotensin II stimulates extracellular matrix protein synthesis through induction of transforming growth factor-beta expression in rat glomerular mesangial cells. J Clin Invest 93:2431–2437
Kajdaniuk D, Marek B, Borgiel-Marek H, Kos-Kudla B (2013) Transforming growth factor beta1 (TGFbeta1) in physiology and pathology. Endokrynol Pol 64:384–396
Kanasaki K, Kanda Y, Palmsten K, Tanjore H, Lee SB, Lebleu VS, Gattone VH Jr, Kalluri R (2008) Integrin beta1-mediated matrix assembly and signaling are critical for the normal development and function of the kidney glomerulus. Dev Biol 313:584–593
Karumanchi SA, Jha V, Ramchandran R, Karihaloo A, Tsiokas L, Chan B, Dhanabal M, Hanai JI, Venkataraman G, Shriver Z, Keiser N, Kalluri R, Zeng H, Mukhopadhyay D, Chen RL, Lander AD, Hagihara K, Yamaguchi Y, Sasisekharan R, Cantley L, Sukhatme VP (2001) Cell surface glypicans are low-affinity endostatin receptors. Mol Cell 7:811–822
Kispert A, Vainio S, Shen L, Rowitch DH, McMahon AP (1996) Proteoglycans are required for maintenance of Wnt-11 expression in the ureter tips. Development 122:3627–3637
Kispert A, Vainio S, McMahon AP (1998) Wnt-4 is a mesenchymal signal for epithelial transformation of metanephric mesenchyme in the developing kidney. Development 125:4225–4234
Kivirikko S, McGrath JA, Pulkkinen L, Uitto J, Christiano AM (1996) Mutational hotspots in the LAMB3 gene in the lethal (Herlitz) type of junctional epidermolysis bullosa. Hum Mol Genet 5:231–237
Kleinman HK, Cannon FB, Laurie GW, Hassell JR, Aumailley M, Terranova VP, Martin GR, DuBois-Dalcq M (1985) Biological activities of laminin. J Cell Biochem 27:317–325
Knoll R, Postel R, Wang J, Kratzner R, Hennecke G, Vacaru AM, Vakeel P, Schubert C, Murthy K, Rana BK, Kube D, Knoll G, Schafer K, Hayashi T, Holm T, Kimura A, Schork N, Toliat MR, Nurnberg P, Schultheiss HP, Schaper W, Schaper J, Bos E, Den Hertog J, van Eeden FJ, Peters PJ, Hasenfuss G, Chien KR, Bakkers J (2007) Laminin-alpha4 and integrin-linked kinase mutations cause human cardiomyopathy via simultaneous defects in cardiomyocytes and endothelial cells. Circulation 116:515–525
Kobayashi A, Valerius MT, Mugford JW, Carroll TJ, Self M, Oliver G, McMahon AP (2008) Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell 3:169–181
Krause M, Rak-Raszewska A, Pietila I, Quaggin SE, Vainio S (2015) Signaling during kidney development. Cell 4:112–132
Kreidberg JA, Donovan MJ, Goldstein SL, Rennke H, Shepherd K, Jones RC, Jaenisch R (1996) Alpha 3 beta 1 integrin has a crucial role in kidney and lung organogenesis. Development 122:3537–3547
Laitinen L, Vartio T, Virtanen I (1991) Cellular fibronectins are differentially expressed in human fetal and adult kidney. Lab Invest 64:492–498
Lampe AK, Bushby KM (2005) Collagen VI related muscle disorders. J Med Genet 42):673–685
Lee V, Singh G, Trasatti JP, Bjornsson C, Xu X, Tran TN, Yoo SS, Dai G, Karande P (2014) Design and fabrication of human skin by three-dimensional bioprinting. Tissue Eng Part C Methods 20:473–484
Lee YB, Polio S, Lee W, Dai G, Menon L, Carroll RS, Yoo SS (2010) Bio-printing of collagen and VEGF-releasing fibrin gel scaffolds for neural stem cell culture. Exp Neurol 223:645–652
Lemmink HH, Nillesen WN, Mochizuki T, Schroder CH, Brunner HG, van Oost BA, Monnens LA, Smeets HJ (1996) Benign familial hematuria due to mutation of the type IV collagen alpha4 gene. J Clin Invest 98:1114–1118
Levett PA, Melchels FP, Schrobback K, Hutmacher DW, Malda J, Klein TJ (2014) A biomimetic extracellular matrix for cartilage tissue engineering centered on photocurable gelatin, hyaluronic acid and chondroitin sulfate. Acta Biomater 10:214–223
Li Q, Williams CG, Sun DD, Wang J, Leong K, Elisseeff JH (2004) Photocrosslinkable polysaccharides based on chondroitin sulfate. J Biomed Mater Res A 68:28–33
Lin S, Gu L (2015) Influence of crosslink density and stiffness on mechanical properties of type I collagen gel. Materials 8:551–560
Lin Y, Zhang S, Rehn M, Itaranta P, Tuukkanen J, Heljasvaara R, Peltoketo H, Pihlajaniemi T, Vainio S (2001) Induced repatterning of type XVIII collagen expression in ureter bud from kidney to lung type: association with sonic hedgehog and ectopic surfactant protein C. Development 128:1573–1585
Lindstrom NO, Hohenstein P, Davies JA (2013) Nephrons require rho-kinase for proximal-distal polarity development. Sci Rep 3:2692
Linton JM, Martin GR, Reichardt LF (2007) The ECM protein nephronectin promotes kidney development via integrin alpha8beta1-mediated stimulation of Gdnf expression. Development 134:2501–2509
Liu S, Yu X, Xu Q, Cui J, Yi M, Zhang X, Ge Y, Ma X (2015) Support of positive association in family-based genetic analysis between COL27A1 and Tourette syndrome. Sci Rep 5:12687
Lyon M, Deakin JA, Mizuno K, Nakamura T, Gallagher JT (1994) Interaction of hepatocyte growth factor with heparan sulfate. Elucidation of the major heparan sulfate structural determinants. J Biol Chem 269:11216–11223
Majava M, Hoornaert KP, Bartholdi D, Bouma MC, Bouman K, Carrera M, Devriendt K, Hurst J, Kitsos G, Niedrist D, Petersen MB, Shears D, Stolte-Dijkstra I, Van Hagen JM, Ala-Kokko L, Mannikko M, Mortier GR (2007) A report on 10 new patients with heterozygous mutations in the COL11A1 gene and a review of genotype-phenotype correlations in type XI collagenopathies. Am J Med Genet A 143A:258–264
Margadant C, Charafeddine RA, Sonnenberg A (2010) Unique and redundant functions of integrins in the epidermis. FASEB J 24:4133–4152
McCright B, Gao X, Shen L, Lozier J, Lan Y, Maguire M, Herzlinger D, Weinmaster G, Jiang R, Gridley T (2001) Defects in development of the kidney, heart and eye vasculature in mice homozygous for a hypomorphic Notch2 mutation. Development 128:491–502
McGrath JA, Kivirikko S, Ciatti S, Moss C, Dunnill GS, Eady RA, Rodeck CH, Christiano AM, Uitto J (1995) A homozygous nonsense mutation in the alpha 3 chain gene of laminin 5 (LAMA3) in Herlitz junctional epidermolysis bullosa: prenatal exclusion in a fetus at risk. Genomics 29:282–284
McLean WH, Irvine AD, Hamill KJ, Whittock NV, Coleman-Campbell CM, Mellerio JE, Ashton GS, Dopping-Hepenstal PJ, Eady RA, Jamil T, Phillips R, Shabbir SG, Haroon TS, Khurshid K, Moore JE, Page B, Darling J, Atherton DJ, Van Steensel MA, Munro CS, Smith FJ, McGrath JA (2003) An unusual N-terminal deletion of the laminin alpha3a isoform leads to the chronic granulation tissue disorder laryngo-onycho-cutaneous syndrome. Hum Mol Genet 12:2395–2409
Mencarelli MA, Heidet L, Storey H, van Geel M, Knebelmann B, Fallerini C, Miglietti N, Antonucci MF, Cetta F, Sayer JA, van den Wijngaard A, Yau S, Mari F, Bruttini M, Ariani F, Dahan K, Smeets B, Antignac C, Flinter F, Renieri A (2015) Evidence of digenic inheritance in Alport syndrome. J Med Genet 52:163–174
Meyer TN, Schwesinger C, Sampogna RV, Vaughn DA, Stuart RO, Steer DL, Bush KT, Nigam SK (2006) Rho kinase acts at separate steps in ureteric bud and metanephric mesenchyme morphogenesis during kidney development. Differentiation 74:638–647
Miner JH (2001) Mystery solved: discovery of a novel integrin ligand in the developing kidney. J Cell Biol 154:257–259
Miner JH, Li C (2000) Defective glomerulogenesis in the absence of laminin alpha5 demonstrates a developmental role for the kidney glomerular basement membrane. Dev Biol 217:278–289
Muller U, Wang D, Denda S, Meneses JJ, Pedersen RA, Reichardt LF (1997) Integrin alpha8beta1 is critically important for epithelial-mesenchymal interactions during kidney morphogenesis. Cell 88:603–613
Muragaki Y, Mariman EC, van Beersum SE, Perala M, van Mourik JB, Warman ML, Olsen BR, Hamel BC (1996) A mutation in the gene encoding the alpha 2 chain of the fibril-associated collagen IX, COL9A2, causes multiple epiphyseal dysplasia (EDM2). Nat Genet 12:103–105
Murphy SV, Atala A (2014) 3D bioprinting of tissues and organs. Nat Biotechnol 32:773–785
Nakayama KH, Lee CC, Batchelder CA, Tarantal AF (2013) Tissue specificity of decellularized rhesus monkey kidney and lung scaffolds. PLoS One 8:e64134
Neelisetty S, Alford C, Reynolds K, Woodbury L, Nlandu-Khodo S, Yang H, Fogo AB, Hao CM, Harris RC, Zent R, Gewin L (2015) Renal fibrosis is not reduced by blocking transforming growth factor-beta signaling in matrix-producing interstitial cells. Kidney Int 88:503–514
Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z (1999) Vascular endothelial growth factor (VEGF) and its receptors. FASEB J 13:9–22
Nicolaou N, Margadant C, Kevelam SH, Lilien MR, Oosterveld MJ, Kreft M, van Eerde AM, Pfundt R, Terhal PA, van der Zwaag B, Nikkels PG, Sachs N, Goldschmeding R, Knoers NV, Renkema KY, Sonnenberg A (2012) Gain of glycosylation in integrin alpha3 causes lung disease and nephrotic syndrome. J Clin Invest 122:4375–4387
Ohuchi H, Hori Y, Yamasaki M, Harada H, Sekine K, Kato S, Itoh N (2000) FGF10 acts as a major ligand for FGF receptor 2 IIIb in mouse multi-organ development. Biochem Biophys Res Commun 277:643–649
Orlando G, Booth C, Wang Z, Totonelli G, Ross CL, Moran E, Salvatori M, Maghsoudlou P, Turmaine M, Delario G, Al-Shraideh Y, Farooq U, Farney AC, Rogers J, Iskandar SS, Burns A, Marini FC, De Coppi P, Stratta RJ, Soker S (2013) Discarded human kidneys as a source of ECM scaffold for kidney regeneration technologies. Biomaterials 34:5915–5925
Ornitz DM (2000) FGFs, heparan sulfate and FGFRs: complex interactions essential for development. BioEssays 22:108–112
Oxburgh L, Brown AC, Muthukrishnan SD, Fetting JL (2014) Bone morphogenetic protein signaling in nephron progenitor cells. Pediatr Nephrol 29:531–536
Pankov R, Yamada KM (2002) Fibronectin at a glance. J Cell Sci 115:3861–3863
Park Y, Lutolf MP, Hubbell JA, Hunziker EB, Wong M (2004) Bovine primary chondrocyte culture in synthetic matrix metalloproteinase-sensitive poly(ethylene glycol)-based hydrogels as a scaffold for cartilage repair. Tissue Eng 10:515–522
Pegoraro E, Fanin M, Trevisan CP, Angelini C, Hoffman EP (2000) A novel laminin alpha2 isoform in severe laminin alpha2 deficient congenital muscular dystrophy. Neurology 55:1128–1134
Perrimon N, Bernfield M (2000) Specificities of heparan sulphate proteoglycans in developmental processes. Nature 404:725–728
Pescosolido L, Schuurman W, Malda J, Matricardi P, Alhaique F, Coviello T, van Weeren PR, Dhert WJ, Hennink WE, Vermonden T (2011) Hyaluronic acid and dextran-based semi-IPN hydrogels as biomaterials for bioprinting. Biomacromolecules 12:1831–1838
Pietila I, Vainio SJ (2014) Kidney development: an overview. Nephron Exp Nephrol 126:40
Pollak MR, Quaggin SE, Hoenig MP, Dworkin LD (2014) The glomerulus: the sphere of influence. Clin J Am Soc Nephrol 9:1461–1469
Poretti A, Hausler M, von Moers A, Baumgartner B, Zerres K, Klein A, Aiello C, Moro F, Zanni G, Santorelli FM, Huisman TA, Weis J, Valente EM, Bertini E, Boltshauser E (2014) Ataxia, intellectual disability, and ocular apraxia with cerebellar cysts: a new disease? Cerebellum 13:79–88
Pozzi A, Jarad G, Moeckel GW, Coffa S, Zhang X, Gewin L, Eremina V, Hudson BG, Borza DB, Harris RC, Holzman LB, Phillips CL, Fassler R, Quaggin SE, Miner JH, Zent R (2008) Beta1 integrin expression by podocytes is required to maintain glomerular structural integrity. Dev Biol 316:288–301
Pulkkinen L, McGrath J, Airenne T, Haakana H, Tryggvason K, Kivirikko S, Meneguzzi G, Ortonne JP, Christiano AM, Uitto J (1997) Detection of novel LAMC2 mutations in Herlitz junctional epidermolysis bullosa. Mol Med 3:124–135
Qiao J, Uzzo R, Obara-Ishihara T, Degenstein L, Fuchs E, Herzlinger D (1999) FGF-7 modulates ureteric bud growth and nephron number in the developing kidney. Development 126:547–554
Rak-Raszewska A, Hauser PV, Vainio S (2015) Organ in vitro culture: what have we learned about early kidney development? Stem Cells Int 2015:959807
Rapraeger AC (2001) Molecular interactions of syndecans during development. Semin Cell Dev Biol 12:107–116
Regoli M, Magro G, Grasso S, Bendayan M (1998) Type VI collagen in glomeruli of short- and long-term experimental diabetic rats. Histochem J 30:13–20
Rodriguez-Fraticelli AE, Martin-Belmonte F (2013) Mechanical control of epithelial lumen formation. Small GTPases 4:136–140
Rosines E, Schmidt HJ, Nigam SK (2007) The effect of hyaluronic acid size and concentration on branching morphogenesis and tubule differentiation in developing kidney culture systems: potential applications to engineering of renal tissues. Biomaterials 28:4806–4817
Ross EA, Williams MJ, Hamazaki T, Terada N, Clapp WL, Adin C, Ellison GW, Jorgensen M, Batich CD (2009) Embryonic stem cells proliferate and differentiate when seeded into kidney scaffolds. J Am Soc Nephrol 20:2338–2347
Rost S, Bach E, Neuner C, Nanda I, Dysek S, Bittner RE, Keller A, Bartsch O, Mlynski R, Haaf T, Muller CR, Kunstmann E (2014) Novel form of X-linked nonsyndromic hearing loss with cochlear malformation caused by a mutation in the type IV collagen gene COL4A6. Eur J Hum Genet 22:208–215
Sachs N, Kreft M, van den Bergh Weerman MA, Beynon AJ, Peters TA, Weening JJ, Sonnenberg A (2006) Kidney failure in mice lacking the tetraspanin CD151. J Cell Biol 175:33–39
Sahoo S, Chung C, Khetan S, Burdick JA (2008) Hydrolytically degradable hyaluronic acid hydrogels with controlled temporal structures. Biomacromolecules 9:1088–1092
Sakai T, Larsen M, Yamada KM (2003) Fibronectin requirement in branching morphogenesis. Nature 423:876–881
Saxen L, Koskimies O, Lahti A, Miettinen H, Rapola J, Wartiovaara J (1968) Differentiation of kidney mesenchyme in an experimental model system. Adv Morphog 7:251–293
Sebinger DD, Ofenbauer A, Gruber P, Malik S, Werner C (2013) ECM modulated early kidney development in embryonic organ culture. Biomaterials 34:6670–6682
Sirin Y, Susztak K (2012) Notch in the kidney: development and disease. J Pathol 226:394–403
Skardal A, Atala A (2015) Biomaterials for integration with 3-D bioprinting. Ann Biomed Eng 43:730–746
Song JJ, Ott HC (2011) Organ engineering based on decellularized matrix scaffolds. Trends Mol Med 17:424–432
Song JJ, Guyette JP, Gilpin SE, Gonzalez G, Vacanti JP, Ott HC (2013) Regeneration and experimental orthotopic transplantation of a bioengineered kidney. Nat Med 19:646–651
Sorokin L, Sonnenberg A, Aumailley M, Timpl R, Ekblom P (1990) Recognition of the laminin E8 cell-binding site by an integrin possessing the alpha 6 subunit is essential for epithelial polarization in developing kidney tubules. J Cell Biol 111:1265–1273
Stark K, Vainio S, Vassileva G, McMahon AP (1994) Epithelial transformation of metanephric mesenchyme in the developing kidney regulated by Wnt-4. Nature 372:679–683
Symoens S, Syx D, Malfait F, Callewaert B, De Backer J, Vanakker O, Coucke P, De Paepe A (2012) Comprehensive molecular analysis demonstrates type V collagen mutations in over 90% of patients with classic EDS and allows to refine diagnostic criteria. Hum Mutat 33:1485–1493
Tomita M, Asada M, Asada N, Nakamura J, Oguchi A, Higashi AY, Endo S, Robertson E, Kimura T, Kita T, Economides AN, Kreidberg J, Yanagita M (2013) Bmp7 maintains undifferentiated kidney progenitor population and determines nephron numbers at birth. PLoS One 8:e73554
Tu C, Cai Q, Yang J, Wan Y, Bei J, Wang S (2003) The fabrication and characterization of poly(lactic acid) scaffolds for tissue engineering by improved solidliquid phase separation. Polym Adv Technol 14:565–573
Vainio S, Lehtonen E, Jalkanen M, Bernfield M, Saxen L (1989) Epithelial-mesenchymal interactions regulate the stage-specific expression of a cell surface proteoglycan, syndecan, in the developing kidney. Dev Biol 134:382–391
Vainio S, Jalkanen M, Bernfield M, Saxen L (1992) Transient expression of syndecan in mesenchymal cell aggregates of the embryonic kidney. Dev Biol 152:221–232
Virtanen I, Laitinen L, Korhonen M (1995) Differential expression of laminin polypeptides in developing and adult human kidney. J Histochem Cytochem 43:621–628
Walker KA, Sims-Lucas S, Bates CM (2016) Fibroblast growth factor receptor signaling in kidney and lower urinary tract development. Pediatr Nephrol 31:885–895
Wang RN, Green J, Wang Z, Deng Y, Qiao M, Peabody M, Zhang Q, Ye J, Yan Z, Denduluri S, Idowu O, Li M, Shen C, Hu A, Haydon RC, Kang R, Mok J, Lee MJ, Luu HL, Shi LL (2014) Bone morphogenetic protein (BMP) signaling in development and human diseases. Genes Dis 1:87–105
Watanabe K, Yamada H, Yamaguchi Y (1995) K-glypican: a novel GPI-anchored heparan sulfate proteoglycan that is highly expressed in developing brain and kidney. J Cell Biol 130:1207–1218
Wolf G, Zahner G, Schroeder R, Stahl RA (1996) Transforming growth factor beta mediates the angiotensin-II-induced stimulation of collagen type IV synthesis in cultured murine proximal tubular cells. Nephrol Dial Transplant 11:263–269
Wu W, Kitamura S, Truong DM, Rieg T, Vallon V, Sakurai H, Bush KT, Vera DR, Ross RS, Nigam SK (2009) Beta1-integrin is required for kidney collecting duct morphogenesis and maintenance of renal function. Am J Physiol Renal Physiol 297:F210–F217
Ye P, Habib SL, Ricono JM, Kim NH, Choudhury GG, Barnes JL, Abboud HE, Arar MY (2004) Fibronectin induces ureteric bud cells branching and cellular cord and tubule formation. Kidney Int 66:1356–1364
Yoneda Y, Haginoya K, Arai H, Yamaoka S, Tsurusaki Y, Doi H, Miyake N, Yokochi K, Osaka H, Kato M, Matsumoto N, Saitsu H (2012) De novo and inherited mutations in COL4A2, encoding the type IV collagen alpha2 chain cause porencephaly. Am J Hum Genet 90:86–90
Zabel B, Hilbert K, Stoss H, Superti-Furga A, Spranger J, Winterpacht A (1996) A specific collagen type II gene (COL2A1) mutation presenting as spondyloperipheral dysplasia. Am J Med Genet 63:123–128
Zallocchi M, Johnson BM, Meehan DT, Delimont D, Cosgrove D (2013) Alpha1beta1 integrin/Rac1-dependent mesangial invasion of glomerular capillaries in Alport syndrome. Am J Pathol 183:1269–1280
Zhang X, Mernaugh G, Yang DH, Gewin L, Srichai MB, Harris RC, Iturregui JM, Nelson RD, Kohan DE, Abrahamson D, Fassler R, Yurchenco P, Pozzi A, Zent R (2009) Beta1 integrin is necessary for ureteric bud branching morphogenesis and maintenance of collecting duct structural integrity. Development 136:3357–3366
Acknowledgements
We thank Patricia Murray (University of Liverpool) for critical reading of the manuscript. This work was supported by grants from the Academy of Finland (263246), Centre of Excellence grant 2012–2017 from the Academy of Finland (251314), Sigrid Jusélius Foundation and CIMO Fellowship (personal grant to G.R.).
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Reint, G., Rak-Raszewska, A. & Vainio, S.J. Kidney development and perspectives for organ engineering. Cell Tissue Res 369, 171–183 (2017). https://doi.org/10.1007/s00441-017-2616-x
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DOI: https://doi.org/10.1007/s00441-017-2616-x