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Expression of Extracellular Matrix Proteins in Basal Membranes During Fetal Nephron Development in Mice

Year 2016, Volume: 37 Issue: 2, 109 - 119, 20.04.2016
https://doi.org/10.17776/csj.10236

Abstract

Abstract. In this study, we investigated the distribution of laminin, collagen type IV, nidogen and fibronectine during metanephric development in fetal mouse kidney by immunohistochemistry. Stain density of basement membranes of tubules, glomerules and mesangial matrix were compared in pre-capillary, immature glomerular and mature glomerular stages of fetal kidney. All the matrix proteins were strongly stained in precapillary stage. In immature glomerular stage, a strong staining was observed for fibronectin. Staining intensity was slightly decreased for the other proteins in this stage. In mature glomerular stage, diminished staining for all proteins was observed similar to the previous stage, except fibronectin. The strongest immunoreactions were found for fibronectin and nidogen in all investigated stages. In general, there was a similar staining intensity for all glycoproteins during maturation except for laminin. It was thought that the distribution of extracellular matrix molecules plays an important role for the kidney development. Interactions amoung these molecules probably crucial on cell behavior like migration, proliferation and differentiation in normal development of the nephron.

Keywords: Fibronectine, Nidogen, Laminin, Collagen type IV, Immunohistochemistry, Fetal Kidney, Mouse

 

 

Özet. Çalışmamızda, fötal fare böbreği metanefrik gelişimde laminin, kollagen tip IV, nidogen ve fibronektin dağılımını imunohistokimyasal olarak inceledik. Tübül, glomerul ve mesangial matriks bazal membran boyanma yoğunluğu, fötal böbreğin pre-kapiller, olgunlaşmamış glomerül ve olgunlaşmış glomerül safhalarında karşılaştırıldı. Matriks proteinlerinin hepsi pre-kapiller safhada koyu boyandı. Olgunlaşmamış glomerül safhasında, fibronektin kuvvetli boyanırken diğer proteinlerin boyanma yoğunluğu azaldı. Olgunlaşmış glomerül safhasında ise fibronektin hariç diğer proteinlerin boyanma yoğunluğu olgunlaşmamış glomerül safhası ile benzerdi. İncelenen tüm safhalarda en yoğun immunreaksiyon nidogen ve fibronektinde bulundu. Genellikle, laminin hariç olgunlaşma boyunca tüm glikoproteinlerin boyanma yoğunluğu benzerdi. Bu, hücreler arası madde proteinlerinin böbrek gelişiminde önemli bir rol oynadığını düşündürmektedir. Muhtemelen bu moleküller arasındaki etkileşimler, normal bir nefron gelişiminde göç, çoğalma ve farklılaşma gibi hücre davranışlarında oldukça önemlidir.

Anahtar Kelimeler: Fibronektin, Nidogen, Laminin, Kollajen tip IV, İmmunohistokimya, Fötal böbrek, Fare

References

  • Hammerman MR, Rogers SA, Ryan G: Growth factors and kidney development. Pediatr Nephrol, 7, 616-620, 1993.
  • Rothenpieler UW, Dressler GR: Pax-2 is required for mesenchyme-to-epithelium conversion during kidney development. Development, 119, 711-720, 1993.
  • Horster MF, Braun GS, Huber SM: Embryonic Renal Epithelia: Induction, Nephrogenesis, and Cell Differentiation. Physiol Rev, 79: 1157-1191, 1999.
  • Sariola H, Holm K, Henke-Fahle S: Early innervation of the metanephric kidney. Development, 104, 589-99, 1988.
  • Platt JL, Trescony P, Lindman B, Oegema TR: Heparin and heparan sulfate delimit nephron formation in fetal metanephric kidneys. Development Biology, 139, 338-48, 1990.
  • Davies J, Lyon M, Gallagher J, Garrod D: Sulphated Proteoglycan is required for Collecting Duct growth and Branching but not Nephron Formation during Kidney Development. Development, 121, 1507-1517, 1995.
  • Qiao J, Cohen D, Herzlinger D: The metanephric blastema differentiates into collecting system and nephron epithelial in vitro. Development, 121, 3207-3214, 1995.
  • Davies JA, Davey MG: Collecting duct morphogenesis. Pediatr Nephrol, 535-541, 1999.
  • Pohl M, Sakurai H, Stuart RO, Nigam SK: Role of hyaluronan and CD44 in in vitro branching morphogenesis of ureteric bud cells. Development Biology, 224, 312-25, 2000.
  • Reilly RF, Ellison H: Mammalian distal tubule: physiology, pathophysiology, and molecular anatom. Physiol Rev, 80, 277-313, 2000.
  • Burrow CR: Regulatory molecules in kidney development. Pediatr Nephrol, 14, 240-253, 2000.
  • Kuure S, Vuolteenaho R, Vainio S: Kidney morphogenesis: cellular and molecular regulation. Mech Dev, 92, 31-45, 2000.
  • Perantoni AO, Dovel LF, Williams CL: Induction of tubules in rat metanephrogenic mesenchyme in the absence of an inductive tissue. Differentiation, 48, 25-31, 1991.
  • Ekblom M, Falk M, Salmivirta K, Durbeej M, Ekblom P: Laminin isoform and epithelial development. Ann N Y Acad Sci, 857, 194-211, 1998.
  • Saxén L: What is needed for kidney differentiation and how do we find it? Int J Dev Biol, 43, 377-380, 1999.
  • Matsuura S, Kondo S, Suga K, Kinoshita Y, Urushihara M, Kagami S: Expression of Focal Adhesion Proteins in the Developing Rat Kidney. J Histochem Cytochem, 59 (9), 864-874, 2011.
  • Lu P, Takai K, Weaver VM, Werb Z: Extracellular Matrix Degradation and Remodeling in Development and Disease. Cold Spring Harb Perspect Biol, 3, 1-24, 2011.
  • Marneros AG, Olsen BR: The role of collagen-derived proteolytic fragments in angiogenesis. Matrix Biol, 20, 337-345, 2001.
  • Hirschi SC, Gray SD, Thibeault SL: Fibronectin: An interesting vocal fold protein. Journal Voice, 16, 310-316, 2002.
  • Hohenester E, Yurchenco PD: Laminins in basement membrane assembly. Cell Adhesion & Migration, 7(1), 1-8, 2013.
  • Bader BL, Smyth N, Nedbal S, Miosge N, Baranowsky A, Mokkapati S, Murshed M, Nischt R: Compound Genetic Ablation of Nidogen 1 and 2 Causes Basement Membrane Defects and Perinatal Lethality in Mice. Mol Cell Biol, 25(15), 6846-6856, 2005.
  • DeLise AM, Fischer L, Tuan RS: Cellular interactions and signaling in cartilage development. Osteoarthritis and cartilage, 8, 309-334, 2000.
  • Brown NH: Extracellular Matrix in Development: Insights from Mechanisms Conserved between Invertebrates and Vertebrates. Cold Spring Harbor Laboratory Press 2011.
  • Sainte-Marie G: A paraffin embedding technique for studies employing immunofluorescence. J Histochem Cytochem, 10, 250-256, 1962.
  • Mounier F, Foidart JM, Gubler MC: Distribution of extracellular matrix glycoproteins during normal development of human kidney, An immunohistochemical study. Lab Invest, 54, 394- 401, 1986.
  • Tuckett F, Morris-Kay G: Alcian blue staining of glycosaminoglycans in embrionic material: Effect of different fixatives. Histochem J, 20, 174-182, 1988.
  • Blanc-Brunat N, Mutin M, Peyrol S: Immunohistochemical localization of type IV collagen fibronectin and laminin in the juxtaglomerular apparatus of the rat kidney. Cell Mol Biol, 35, 469-484, 1989.
  • Soto-Suazo M, Abrahamsohn PA, Pereda J, Zorn TMT: Distribution and space-time relationship of proteoglycans in the extracellular matrix of the migratory pathway of primordial germ cells in mouse embryos. Tissue and Cell, 31, 291-300, 1999.
  • Pöschl E, Schlötzer-Schrehardt U, Brachvogel B, Saito K, Ninomiya Y, Mayer U: Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development, 131, 1619-1628, 2004.
  • Leitinger B: Transmembrane Collagen Receptors. Annual Review of Cell and Developmental Biolog, 27, 265-290, 2011.
  • Desjardins M, Bendayan M: Heterogeneous distribution of type IV collagen, entactin, heparan sulfate proteoglycan, and laminin among renal basement membranes as demonstrated by quantitative immunocytochemistry. J Histochem Cytochem, 37, 885- 897,1989.
  • Desjardins M, Gros F, Wieslander J, Gubler MC, Bendayan M: Heterogeneous distribution of monomeric elements from the globular domain (NC1) of type IV collagen in renal basement as revealed by high resolution quantitative immunocytochemistry. Lab Invest, 63: 637-646, 1990.
  • Couchman JR: Heterogeneous distribution of a basement membrane heparan sulfate proteoglycan in rat tissue. J Cell Biol, 105, 1901-1916, 1987.
  • Desjardins M, Bendayan M: Ontogenesis of glomerular basement membrane: Structural and functional properties. J Cell Biol, 113, 689-700, 1991.
  • Abrahamson DR, St. John PL: Laminin distribution in developing glomerular basement membranes. Kidney Int, 43, 73-8, 1993.
  • Michael AF, Yang JY, Falk RJ, Bennington MJ, Scheinman JI, Vernier RL, Fish AJ: Monoclonal antibodies to human renal basement membranes: heterogenic and ontogenic changes. Kidney Int, 24, 74 -86, 1983.
  • Alvarez-Buylla A, Merchant-Larious H: Mouse primordial germ cells use fibronectin as a substrate for migration. Exp Cell Res,165, 362-8, 1986.
  • Ffrench-Constant C, Hollingsworth A, Heasman J, Wylie CC: Response to fibronectin of mouse primordial germ cells before, during and after migration. Development, 113, 1365- 73, 1991.
  • Miosge N, Köther F, Heinemann S, Kohfeldt E, Herken R, Timpl R: Ultrastructural colocalization of nidogen-1 and nidogen-2 with laminin-1 in murine kidney basement membranes. Histochem Cell Biol, 113, 115-24, 2000.
  • Cheignon M, Bakala H, Cornet S, Djaziri R, Schaeverbeke J: Localization of basement membrane glycoproteins in rat kidney during foetal development. Biol Cell, 60, 49-56, 1987.
  • Maric C, Ryan GB, Alcorn D: Embryonic and postnatal development of the rat renal interstitium. Anat Embryol (Berl), 195, 503-14, 1997.
  • Harvey SJ, Zheng K, Sado Y, Naito I, Ninomiya Y, Jacobs RM, Hudson BG, Thorner PS: Role of distinct type IV collagen networks in glomerular development and function. Kidney Int, 54, 1857-1866, 1998.
  • Abrahamson DR, Prettyman AC, Robert B, St. John PL: Laminin-1 reexpression in Alport mouse glomerular basement membranes. Kidney Int, 63, 826-34, 2003.
  • Piepenhagen PA, Nelson WJ: Biogenesis of polarized epithelial cells during kidney development in situ: roles of E-cadherin-mediated cell-cell adhesion and membrane cytoskeleton organization. Mol Biol Cell,11, 3161-77, 1998.
  • Aumailley M, Battagllia C, Mayer U, Reinhardt D, Nischt R, Timpl R, Fox JW: Nidogen mediates the formation of ternary complexes of basement membrane components. Kidney Int, 43, 7-12, 1993.
  • Dziadek M: Role of laminin-nidogen complexes in basement membrane formation during embryonic development. Experientia, 51, 901-913, 1995.
  • Ryan MC, Christiano AM, Engvall E, Wewer UM, Miner JH, Saner JR, Burgeson RE: The functions of laminins: Lessons from in vivo studies. Matrix Biol, 15, 369-381, 1996.
  • Sebinger DD, Ofenbauer A, Gruber P, Malik S, Werner C: ECM modulated early kidney development in embryonic organ culture. Biomaterials, 28, 6670-82, 2013.

During Fetal Nephron Development in Mice

Year 2016, Volume: 37 Issue: 2, 109 - 119, 20.04.2016
https://doi.org/10.17776/csj.10236

Abstract

Çalışmamızda, fötal fare böbreği metanefrik gelişimde laminin, kollagen tip IV, nidogen ve fibronektin dağılımını imunohistokimyasal olarak inceledik. Tübül, glomerul ve mesangial matriks bazal membran boyanma yoğunluğu, fötal böbreğin pre- kapiller, olgunlaşmamış glomerül ve olgunlaşmış glomerül safhalarında karşılaştırıldı. Matriks proteinlerinin hepsi pre-kapiller safhada koyu boyandı. Olgunlaşmamış glomerül safhasında, fibronektin kuvvetli boyanırken diğer proteinlerin boyanma yoğunluğu azaldı. Olgunlaşmış glomerül safhasında ise fibronektin hariç diğer proteinlerin boyanma yoğunluğu olgunlaşmamış glomerül safhası ile benzerdi. İncelenen tüm safhalarda en yoğun immunreaksiyon nidogen ve fibronektinde bulundu. Genellikle, laminin hariç olgunlaşma boyunca tüm glikoproteinlerin boyanma yoğunluğu benzerdi. Bu, hücreler arası madde proteinlerinin böbrek gelişiminde önemli bir rol oynadığını düşündürmektedir. Muhtemelen bu moleküller arasındaki etkileşimler, normal bir nefron gelişiminde göç, çoğalma ve farklılaşma gibi hücre davranışlarında oldukça önemlidir

References

  • Hammerman MR, Rogers SA, Ryan G: Growth factors and kidney development. Pediatr Nephrol, 7, 616-620, 1993.
  • Rothenpieler UW, Dressler GR: Pax-2 is required for mesenchyme-to-epithelium conversion during kidney development. Development, 119, 711-720, 1993.
  • Horster MF, Braun GS, Huber SM: Embryonic Renal Epithelia: Induction, Nephrogenesis, and Cell Differentiation. Physiol Rev, 79: 1157-1191, 1999.
  • Sariola H, Holm K, Henke-Fahle S: Early innervation of the metanephric kidney. Development, 104, 589-99, 1988.
  • Platt JL, Trescony P, Lindman B, Oegema TR: Heparin and heparan sulfate delimit nephron formation in fetal metanephric kidneys. Development Biology, 139, 338-48, 1990.
  • Davies J, Lyon M, Gallagher J, Garrod D: Sulphated Proteoglycan is required for Collecting Duct growth and Branching but not Nephron Formation during Kidney Development. Development, 121, 1507-1517, 1995.
  • Qiao J, Cohen D, Herzlinger D: The metanephric blastema differentiates into collecting system and nephron epithelial in vitro. Development, 121, 3207-3214, 1995.
  • Davies JA, Davey MG: Collecting duct morphogenesis. Pediatr Nephrol, 535-541, 1999.
  • Pohl M, Sakurai H, Stuart RO, Nigam SK: Role of hyaluronan and CD44 in in vitro branching morphogenesis of ureteric bud cells. Development Biology, 224, 312-25, 2000.
  • Reilly RF, Ellison H: Mammalian distal tubule: physiology, pathophysiology, and molecular anatom. Physiol Rev, 80, 277-313, 2000.
  • Burrow CR: Regulatory molecules in kidney development. Pediatr Nephrol, 14, 240-253, 2000.
  • Kuure S, Vuolteenaho R, Vainio S: Kidney morphogenesis: cellular and molecular regulation. Mech Dev, 92, 31-45, 2000.
  • Perantoni AO, Dovel LF, Williams CL: Induction of tubules in rat metanephrogenic mesenchyme in the absence of an inductive tissue. Differentiation, 48, 25-31, 1991.
  • Ekblom M, Falk M, Salmivirta K, Durbeej M, Ekblom P: Laminin isoform and epithelial development. Ann N Y Acad Sci, 857, 194-211, 1998.
  • Saxén L: What is needed for kidney differentiation and how do we find it? Int J Dev Biol, 43, 377-380, 1999.
  • Matsuura S, Kondo S, Suga K, Kinoshita Y, Urushihara M, Kagami S: Expression of Focal Adhesion Proteins in the Developing Rat Kidney. J Histochem Cytochem, 59 (9), 864-874, 2011.
  • Lu P, Takai K, Weaver VM, Werb Z: Extracellular Matrix Degradation and Remodeling in Development and Disease. Cold Spring Harb Perspect Biol, 3, 1-24, 2011.
  • Marneros AG, Olsen BR: The role of collagen-derived proteolytic fragments in angiogenesis. Matrix Biol, 20, 337-345, 2001.
  • Hirschi SC, Gray SD, Thibeault SL: Fibronectin: An interesting vocal fold protein. Journal Voice, 16, 310-316, 2002.
  • Hohenester E, Yurchenco PD: Laminins in basement membrane assembly. Cell Adhesion & Migration, 7(1), 1-8, 2013.
  • Bader BL, Smyth N, Nedbal S, Miosge N, Baranowsky A, Mokkapati S, Murshed M, Nischt R: Compound Genetic Ablation of Nidogen 1 and 2 Causes Basement Membrane Defects and Perinatal Lethality in Mice. Mol Cell Biol, 25(15), 6846-6856, 2005.
  • DeLise AM, Fischer L, Tuan RS: Cellular interactions and signaling in cartilage development. Osteoarthritis and cartilage, 8, 309-334, 2000.
  • Brown NH: Extracellular Matrix in Development: Insights from Mechanisms Conserved between Invertebrates and Vertebrates. Cold Spring Harbor Laboratory Press 2011.
  • Sainte-Marie G: A paraffin embedding technique for studies employing immunofluorescence. J Histochem Cytochem, 10, 250-256, 1962.
  • Mounier F, Foidart JM, Gubler MC: Distribution of extracellular matrix glycoproteins during normal development of human kidney, An immunohistochemical study. Lab Invest, 54, 394- 401, 1986.
  • Tuckett F, Morris-Kay G: Alcian blue staining of glycosaminoglycans in embrionic material: Effect of different fixatives. Histochem J, 20, 174-182, 1988.
  • Blanc-Brunat N, Mutin M, Peyrol S: Immunohistochemical localization of type IV collagen fibronectin and laminin in the juxtaglomerular apparatus of the rat kidney. Cell Mol Biol, 35, 469-484, 1989.
  • Soto-Suazo M, Abrahamsohn PA, Pereda J, Zorn TMT: Distribution and space-time relationship of proteoglycans in the extracellular matrix of the migratory pathway of primordial germ cells in mouse embryos. Tissue and Cell, 31, 291-300, 1999.
  • Pöschl E, Schlötzer-Schrehardt U, Brachvogel B, Saito K, Ninomiya Y, Mayer U: Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development, 131, 1619-1628, 2004.
  • Leitinger B: Transmembrane Collagen Receptors. Annual Review of Cell and Developmental Biolog, 27, 265-290, 2011.
  • Desjardins M, Bendayan M: Heterogeneous distribution of type IV collagen, entactin, heparan sulfate proteoglycan, and laminin among renal basement membranes as demonstrated by quantitative immunocytochemistry. J Histochem Cytochem, 37, 885- 897,1989.
  • Desjardins M, Gros F, Wieslander J, Gubler MC, Bendayan M: Heterogeneous distribution of monomeric elements from the globular domain (NC1) of type IV collagen in renal basement as revealed by high resolution quantitative immunocytochemistry. Lab Invest, 63: 637-646, 1990.
  • Couchman JR: Heterogeneous distribution of a basement membrane heparan sulfate proteoglycan in rat tissue. J Cell Biol, 105, 1901-1916, 1987.
  • Desjardins M, Bendayan M: Ontogenesis of glomerular basement membrane: Structural and functional properties. J Cell Biol, 113, 689-700, 1991.
  • Abrahamson DR, St. John PL: Laminin distribution in developing glomerular basement membranes. Kidney Int, 43, 73-8, 1993.
  • Michael AF, Yang JY, Falk RJ, Bennington MJ, Scheinman JI, Vernier RL, Fish AJ: Monoclonal antibodies to human renal basement membranes: heterogenic and ontogenic changes. Kidney Int, 24, 74 -86, 1983.
  • Alvarez-Buylla A, Merchant-Larious H: Mouse primordial germ cells use fibronectin as a substrate for migration. Exp Cell Res,165, 362-8, 1986.
  • Ffrench-Constant C, Hollingsworth A, Heasman J, Wylie CC: Response to fibronectin of mouse primordial germ cells before, during and after migration. Development, 113, 1365- 73, 1991.
  • Miosge N, Köther F, Heinemann S, Kohfeldt E, Herken R, Timpl R: Ultrastructural colocalization of nidogen-1 and nidogen-2 with laminin-1 in murine kidney basement membranes. Histochem Cell Biol, 113, 115-24, 2000.
  • Cheignon M, Bakala H, Cornet S, Djaziri R, Schaeverbeke J: Localization of basement membrane glycoproteins in rat kidney during foetal development. Biol Cell, 60, 49-56, 1987.
  • Maric C, Ryan GB, Alcorn D: Embryonic and postnatal development of the rat renal interstitium. Anat Embryol (Berl), 195, 503-14, 1997.
  • Harvey SJ, Zheng K, Sado Y, Naito I, Ninomiya Y, Jacobs RM, Hudson BG, Thorner PS: Role of distinct type IV collagen networks in glomerular development and function. Kidney Int, 54, 1857-1866, 1998.
  • Abrahamson DR, Prettyman AC, Robert B, St. John PL: Laminin-1 reexpression in Alport mouse glomerular basement membranes. Kidney Int, 63, 826-34, 2003.
  • Piepenhagen PA, Nelson WJ: Biogenesis of polarized epithelial cells during kidney development in situ: roles of E-cadherin-mediated cell-cell adhesion and membrane cytoskeleton organization. Mol Biol Cell,11, 3161-77, 1998.
  • Aumailley M, Battagllia C, Mayer U, Reinhardt D, Nischt R, Timpl R, Fox JW: Nidogen mediates the formation of ternary complexes of basement membrane components. Kidney Int, 43, 7-12, 1993.
  • Dziadek M: Role of laminin-nidogen complexes in basement membrane formation during embryonic development. Experientia, 51, 901-913, 1995.
  • Ryan MC, Christiano AM, Engvall E, Wewer UM, Miner JH, Saner JR, Burgeson RE: The functions of laminins: Lessons from in vivo studies. Matrix Biol, 15, 369-381, 1996.
  • Sebinger DD, Ofenbauer A, Gruber P, Malik S, Werner C: ECM modulated early kidney development in embryonic organ culture. Biomaterials, 28, 6670-82, 2013.
There are 48 citations in total.

Details

Journal Section Natural Sciences Research Article
Authors

Beyhan Gürcü

İbrahim Tuğlu This is me

Sabire Karaçalı This is me

Publication Date April 20, 2016
Published in Issue Year 2016 Volume: 37 Issue: 2

Cite

APA Gürcü, B., Tuğlu, İ., & Karaçalı, S. (2016). Expression of Extracellular Matrix Proteins in Basal Membranes During Fetal Nephron Development in Mice. Cumhuriyet Üniversitesi Fen Edebiyat Fakültesi Fen Bilimleri Dergisi, 37(2), 109-119. https://doi.org/10.17776/csj.10236
AMA Gürcü B, Tuğlu İ, Karaçalı S. Expression of Extracellular Matrix Proteins in Basal Membranes During Fetal Nephron Development in Mice. Cumhuriyet Üniversitesi Fen Edebiyat Fakültesi Fen Bilimleri Dergisi. April 2016;37(2):109-119. doi:10.17776/csj.10236
Chicago Gürcü, Beyhan, İbrahim Tuğlu, and Sabire Karaçalı. “Expression of Extracellular Matrix Proteins in Basal Membranes During Fetal Nephron Development in Mice”. Cumhuriyet Üniversitesi Fen Edebiyat Fakültesi Fen Bilimleri Dergisi 37, no. 2 (April 2016): 109-19. https://doi.org/10.17776/csj.10236.
EndNote Gürcü B, Tuğlu İ, Karaçalı S (April 1, 2016) Expression of Extracellular Matrix Proteins in Basal Membranes During Fetal Nephron Development in Mice. Cumhuriyet Üniversitesi Fen Edebiyat Fakültesi Fen Bilimleri Dergisi 37 2 109–119.
IEEE B. Gürcü, İ. Tuğlu, and S. Karaçalı, “Expression of Extracellular Matrix Proteins in Basal Membranes During Fetal Nephron Development in Mice”, Cumhuriyet Üniversitesi Fen Edebiyat Fakültesi Fen Bilimleri Dergisi, vol. 37, no. 2, pp. 109–119, 2016, doi: 10.17776/csj.10236.
ISNAD Gürcü, Beyhan et al. “Expression of Extracellular Matrix Proteins in Basal Membranes During Fetal Nephron Development in Mice”. Cumhuriyet Üniversitesi Fen Edebiyat Fakültesi Fen Bilimleri Dergisi 37/2 (April 2016), 109-119. https://doi.org/10.17776/csj.10236.
JAMA Gürcü B, Tuğlu İ, Karaçalı S. Expression of Extracellular Matrix Proteins in Basal Membranes During Fetal Nephron Development in Mice. Cumhuriyet Üniversitesi Fen Edebiyat Fakültesi Fen Bilimleri Dergisi. 2016;37:109–119.
MLA Gürcü, Beyhan et al. “Expression of Extracellular Matrix Proteins in Basal Membranes During Fetal Nephron Development in Mice”. Cumhuriyet Üniversitesi Fen Edebiyat Fakültesi Fen Bilimleri Dergisi, vol. 37, no. 2, 2016, pp. 109-1, doi:10.17776/csj.10236.
Vancouver Gürcü B, Tuğlu İ, Karaçalı S. Expression of Extracellular Matrix Proteins in Basal Membranes During Fetal Nephron Development in Mice. Cumhuriyet Üniversitesi Fen Edebiyat Fakültesi Fen Bilimleri Dergisi. 2016;37(2):109-1.