Ⅰ型胶原诱导骨髓间充质干细胞及成骨细胞的成骨分化机制
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摘要
背景:Ⅰ型胶原为骨组织细胞外基质的主要成分,多项研究表明其具有诱导成骨分化的能力,其在骨组织矿化过程中起着重要的作用,目前生物材料领域正致力研究替代Ⅰ型胶原的仿生材料。目的:综述Ⅰ型胶原诱导成骨的机制,在生物矿化过程中的作用及在牵张成骨过程中的实时表达。方法:检索CNKI数据库和Pub Med数据库检索1990至2017年期间关于Ⅰ型胶原诱导成骨、牵张成骨Ⅰ型胶原表达及生物矿化的文章,检索词分别为"Ⅰ型胶原(Ⅰ型胶原蛋白),骨髓间充质干细胞,成骨细胞,牵张成骨,生物矿化"和"type Ⅰ collagen,bone marrow mesenchymal stem cells,osteoblast,distraction osteogenesis,mineralization",最后选择58篇文章纳入结果分析。结果与结论:(1)Ⅰ型胶原诱导骨髓间充质干细胞及成骨细胞成骨分化主要通过胶原-整合素信号通道;(2)在牵张成骨早期Ⅰ型胶原分泌较少,中后期分泌较多,成为细胞外主要基质;(3)矿化机制目前主流2种学说:Ⅰ型胶原在生物矿化中起到模板支架作用,引导钙盐沉积、矿化;无定形磷酸钙无机质渗入胶原纤维之间,由非晶体状态转为晶体状态,形成定向排列晶体结构。
BACKGROUND: Type I collagen is the main component of the extracellular matrix of bone tissue. Numerous studies have shown that it has the ability to induce osteogenic differentiation, and plays an important role in the process of bone mineralization. Currently, bionic materials are being developed as an alternative to type Ⅰ collagen in the field of biological materials.OBJECTIVE: To review the mechanism of osteogenesis induced by type Ⅰ collagen, the role of type Ⅰ collagen in the biomineralization process, and the real-time expression of type Ⅰ collagen during distraction osteogenesis. METHODS: With the key words of "type Ⅰ collagen, bone marrow mesenchymal stem cells, osteoblast, distractionosteogenesis, mineralization" in Chinese and English, we performed a computer-based search in CNKI and Pub Med database for relevant articles published from 1990 to 2017. Finally, 58 eligible articles were included in result analysis. RESULTS AND CONCLUSION: Type I collagen induces osteogenic differentiation of bone marrow mesenchymal stem cells and osteoblasts mainly through collagen-integrin signaling pathways. In the early stage of distraction osteogenesis, type Ⅰ collagen is less secreted, but the secretion increases in the middle and later stages, eventually becoming the main component of extracellular matrix. There are two mainstream theories of mineralization mechanisms:(1) Type I collagen plays a role as a template scaffold in biomineralization, guiding the deposition and mineralization of calcium.(2) Amorphous calcium phosphate infiltrates between collagen fibers and changes from amorphous to crystalline state, forming an aligned crystal structure.
BACKGROUND: Type I collagen is the main component of the extracellular matrix of bone tissue. Numerous studies have shown that it has the ability to induce osteogenic differentiation, and plays an important role in the process of bone mineralization. Currently, bionic materials are being developed as an alternative to type Ⅰ collagen in the field of biological materials.OBJECTIVE: To review the mechanism of osteogenesis induced by type Ⅰ collagen, the role of type Ⅰ collagen in the biomineralization process, and the real-time expression of type Ⅰ collagen during distraction osteogenesis. METHODS: With the key words of "type Ⅰ collagen, bone marrow mesenchymal stem cells, osteoblast, distractionosteogenesis, mineralization" in Chinese and English, we performed a computer-based search in CNKI and Pub Med database for relevant articles published from 1990 to 2017. Finally, 58 eligible articles were included in result analysis. RESULTS AND CONCLUSION: Type I collagen induces osteogenic differentiation of bone marrow mesenchymal stem cells and osteoblasts mainly through collagen-integrin signaling pathways. In the early stage of distraction osteogenesis, type Ⅰ collagen is less secreted, but the secretion increases in the middle and later stages, eventually becoming the main component of extracellular matrix. There are two mainstream theories of mineralization mechanisms:(1) Type I collagen plays a role as a template scaffold in biomineralization, guiding the deposition and mineralization of calcium.(2) Amorphous calcium phosphate infiltrates between collagen fibers and changes from amorphous to crystalline state, forming an aligned crystal structure.
引文
[1]Gordon MK,Hahn RA.Collagens.Cell Tissue Res.2010;339(1):247-257.
[2]Roche P,Czubryt MP.Transcriptional control of collagen I gene expression.Cardiovasc Hematol Disord Drug Targets.2014;14(2):107-120.
[3]Vuorio E,de Crombrugghe B.The family of collagen genes.Annu Rev Biochem.1990;59:837-872.
[4]Jimenez SA,Varga J,Olsen A,et al.Functional analysis of human alpha 1(Ⅰ)procollagen gene promoter.Differential activity in collagen-producing and-nonproducing cells and response to transforming growth factor beta 1.J Biol Chem.1994;269(17):12684-12691.
[5]Ghosh AK,Yuan W,Mori Y,et al.Antagonistic regulation of type Ⅰ collagen gene expression by interferon-gamma and transforming growth factor-beta.Integration at the level of p300/CBP transcriptional coactivators.J Biol Chem.2001;276(14):11041-11048.
[6]Canty EG,Kadler KE.Procollagen trafficking,processing and fibrillogenesis.J Cell Sci.2005;118(Pt 7):1341-1353.
[7]Tasab M,Batten MR,Bulleid NJ.Hsp47:a molecular chaperone that interacts with and stabilizes correctly-folded procollagen.EMBO J.2000;19(10):2204-2211.
[8]Sauk JJ,Norris K,Hebert C,et al.Hsp47 binds to the KDEL receptor and cell surface expression is modulated by cytoplasmic and endosomal p H.Connect Tissue Res.1998;37(1-2):105-119.
[9]Ishikawa Y,B?chinger HP.A molecular ensemble in the r ER for procollagen maturation.Biochim Biophys Acta.2013;1833(11):2479-2491.
[10]Garnero P.Erratum to:The Role of Collagen Organization on the Properties of Bone.Calcif Tissue Int.2015;97(3):241.
[11]Cohen-Solal L,Zylberberg L,Sangalli A,et al.Substitution of an aspartic acid for glycine 700 in the alpha 2(I)chain of type Ⅰ collagen in a recurrent lethal type ⅠI osteogenesis imperfecta dramatically affects the mineralization of bone.J Biol Chem.1994;269(20):14751-14758.
[12]Bardai G,Lemyre E,Moffatt P,et al.Osteogenesis Imperfecta Type Ⅰ Caused by COL1A1 Deletions.Calcif Tissue Int.2016;98(1):76-84.
[13]Prockop DJ.Mutations that alter the primary structure of type Ⅰ collagen.The perils of a system for generating large structures by the principle of nucleated growth.J Biol Chem.1990;265(26):15349-15352.
[14]Gerhard DS,Wagner L,Feingold EA,et al.The status,quality,and expansion of the NIH full-length c DNA project:the Mammalian Gene Collection(MGC).Genome Res.2004;14(10B):2121-2127.
[15]He W,Wu WK,Wu YL,et al.Ginsenoside-Rg1 mediates microenvironment-dependent endothelial differentiation of human mesenchymal stem cells in vitro.J Asian Nat Prod Res.2011;13(1):1-11.
[16]Mizuno M,Fujisawa R,Kuboki Y.Type Ⅰ collagen-induced osteoblastic differentiation of bone-marrow cells mediated by collagen-alpha2beta1 integrin interaction.J Cell Physiol.2000;184(2):207-213.
[17]Bortell R,Barone LM,Tassinari MS,et al.Gene expression during endochondral bone development:evidence for coordinate expression of transforming growth factor beta 1and collagen type Ⅰ.J Cell Biochem.1990;44(2):81-91.
[18]Pittenger MF,Mackay AM,Beck SC,et al.Multilineage potential of adult human mesenchymal stem cells.Science.1999;284(5411):143-147.
[19]Aronow MA,Gerstenfeld LC,Owen TA,et al.Factors that promote progressive development of the osteoblast phenotype in cultured fetal rat calvaria cells.J Cell Physiol.1990;143(2):213-221.
[20]Hesse E,Hefferan TE,Tarara JE,et al.Collagen type Ⅰ hydrogel allows migration,proliferation,and osteogenic differentiation of rat bone marrow stromal cells.J Biomed Mater Res A.2010;94(2):442-449.
[21]Mizuno M,Kuboki Y.Osteoblast-related gene expression of bone marrow cells during the osteoblastic differentiation induced by type Ⅰ collagen.J Biochem.2001;129(1):133-138.
[22]Linsley C,Wu B,Tawil B.The effect of fibrinogen,collagen type Ⅰ,and fibronectin on mesenchymal stem cell growth and differentiation into osteoblasts.Tissue Eng Part A.2013;19(11-12):1416-1423.
[23]Salomon DS.Cell-cell and cell-extracellular matrix adhesion molecules communicate with growth factor receptors:an interactive signaling Web.Cancer Invest.2000;18(6):591-593.
[24]Staatz WD,Fok KF,Zutter MM,et al.Identification of a tetrapeptide recognition sequence for the alpha 2 beta 1integrin in collagen.J Biol Chem.1991;266(12):7363-7367.
[25]Puklin-Faucher E,Sheetz MP.The mechanical integrin cycle.J Cell Sci.2009;122(Pt 2):179-186.
[26]Schwartz MA.Integrins,oncogenes,and anchorage independence.J Cell Biol.1997;139(3):575-578.
[27]Wen LP,Fahrni JA,Troie S,et al.Cleavage of focal adhesion kinase by caspases during apoptosis.J Biol Chem.1997;272(41):26056-26061.
[28]Kim EK,Choi EJ.Pathological roles of MAPK signaling pathways in human diseases.Biochim Biophys Acta.2010;1802(4):396-405.
[29]Salasznyk RM,Klees RF,Williams WA,et al.Focal adhesion kinase signaling pathways regulate the osteogenic differentiation of human mesenchymal stem cells.Exp Cell Res.2007;313(1):22-37
[30]Jadlowiec J,Koch H,Zhang X,et al.Phosphophoryn regulates the gene expression and differentiation of NIH3T3,MC3T3-E1,and human mesenchymal stem cells via the integrin/MAPK signaling pathway.J Biol Chem.2004;279(51):53323-53330.
[31]Stein GS,Lian JB,Stein JL,et al.Transcriptional control of osteoblast growth and differentiation.Physiol Rev.1996;76(2):593-629.
[32]Ganta DR,Mc Carthy MB,Gronowicz GA.Ascorbic acid alters collagen integrins in bone culture.Endocrinology.1997;138(9):3606-3612.
[33]杨志明,屈艺.Ⅰ型胶原—整合素α2β1系统对成骨细胞生物学特性的调控[J].四川大学学报:医学版,2000,31(3):281-284.
[34]Wenstrup RJ,Witte DP,Florer JB.Abnormal differentiation in MC3T3-E1 preosteoblasts expressing a dominant-negative type Ⅰ collagen mutation.Connect Tissue Res.1996;35(1-4):249-257.
[35]Mofid MM,Manson PN,Robertson BC,et al.Craniofacial distraction osteogenesis:a review of 3278 cases.Plast Reconstr Surg.2001;108(5):1103-1114.
[36]Schreuder WH,Jansma J,Bierman MW,et al.Distraction osteogenesis versus bilateral sagittal split osteotomy for advancement of the retrognathic mandible:a review of the literature.Int J Oral Maxillofac Surg.2007;36(2):103-110.
[37]王大章,陈刚,胡静.牵张成骨在矫治牙颌面畸形中的应用[J].华西口腔医学杂志,1998,5(4):369-371.
[38]Welch RD,Lewis DD.Distraction osteogenesis.Vet Clin North Am Small Anim Pract.1999,29(5):1187-1205.
[39]柴本甫,汤雪明.实验性骨折愈合的细胞生物学[J].中华骨科杂志,1991,11(3):203-206.
[40]韦敏,穆雄铮,张涤生,等.颅面牵拉成骨胶原合成的研究[J].口腔颌面外科杂志,2001,11(1):32-34.
[41]丁宇翔,刘彦普,敖建华.牙槽突裂牵张成骨胶原合成的研究[J].实用口腔医学杂志,2005,21(4):477-479.
[42]商洪涛,刘锐,孙建壮,等.上颌骨缝牵张的组织学变化[J].中国组织工程研究,2007,11(10):1833-1836.
[43]Chen X,Li N,Lele Yang,et al.Expression of collagen I,collagen III and MMP-1 on the tension side of distracted tooth using periodontal ligament distraction osteogenesis in beagle dogs.Arch Oral Biol.2014;59(11):1217-1225.
[44]姜喜亮,朱晓文,胡静,等.整合素信号通路在大鼠骨髓间充质干细胞牵张中的作用和转导机制[J].中国口腔颌面外科杂志,2015,13(3):193-199.
[45]Liebschner MA.Biomechanical considerations of animal models used in tissue engineering of bone.Biomaterials.2004;25(9):1697-1714.
[46]Cisneros DA,Hung C,Franz CM,et al.Observing growth steps of collagen self-assembly by time-lapse high-resolution atomic force microscopy.J Struct Biol.2006;154(3):232-345.
[47]Olszta MJ,Cheng X,Sang SJ,et al.Bone structure and formation:A new perspective.Materials Science&Engineering R.2008;58(3):77-116.
[48]Xu Z,Yang Y,Zhao W,et al.Molecular mechanisms for intrafibrillar collagen mineralization in skeletal tissues.Biomaterials.2015;39:59-66.
[49]Wei Z,Huang ZL,Liao SS,et al.Nucleation Sites of Calcium Phosphate Crystals during Collagen Mineralization.Journal of the American Ceramic Society.2003;86(6):1052-1054.
[50]涂姜磊,郭富强,吕春春,等.胶原诱导沉积类骨HA及其机制研究[J].生物医学工程学杂志,2011,28(1):99-103.
[51]Nudelman F,Pieterse K,George A,et al.The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors.Nat Mater.2010;9(12):1004-1009.
[52]Cantaert B,Kim YY,Ludwig H,et al.Think Positive:Phase Separation Enables a Positively Charged Additive to Induce Dramatic Changes in Calcium Carbonate Morphology.Advanced Functional Materials.2012;22(5):907-915.
[53]Zurick KM,Qin C,Bernards MT.Mineralization induction effects of osteopontin,bone sialoprotein,and dentin phosphoprotein on a biomimetic collagen substrate.J Biomed Mater Res A.2013;101(6):1571-1581.
[54]Qiu ZY,Cui Y,Tao CS,et al.Mineralized Collagen:Rationale,Current Status,and Clinical Applications.Materials(Basel).2015;8(8):4733-4750.
[55]Kerns JG,Buckley K,Churchwell J,et al.Is the Collagen Primed for Mineralization in Specific Regions of the Turkey Tendon?An Investigation of the Protein-Mineral Interface Using Raman Spectroscopy.Anal Chem.2016;88(3):1559-1563.
[56]Wang Y,Aza?s T,Robin M,et al.The predominant role of collagen in the nucleation,growth,structure and orientation of bone apatite.Nat Mater.2012;11(8):724-733.
[57]Hvistendahl M.China's push in tissue engineering.Science.2012;338(6109):900-902.
[58]Kumar MS,Kirubanandan S,Sripriya R,et al.Triphala incorporated collagen sponge--a smart biomaterial for infected dermal wound healing.J Surg Res.2010;158(1):162-170.
[2]Roche P,Czubryt MP.Transcriptional control of collagen I gene expression.Cardiovasc Hematol Disord Drug Targets.2014;14(2):107-120.
[3]Vuorio E,de Crombrugghe B.The family of collagen genes.Annu Rev Biochem.1990;59:837-872.
[4]Jimenez SA,Varga J,Olsen A,et al.Functional analysis of human alpha 1(Ⅰ)procollagen gene promoter.Differential activity in collagen-producing and-nonproducing cells and response to transforming growth factor beta 1.J Biol Chem.1994;269(17):12684-12691.
[5]Ghosh AK,Yuan W,Mori Y,et al.Antagonistic regulation of type Ⅰ collagen gene expression by interferon-gamma and transforming growth factor-beta.Integration at the level of p300/CBP transcriptional coactivators.J Biol Chem.2001;276(14):11041-11048.
[6]Canty EG,Kadler KE.Procollagen trafficking,processing and fibrillogenesis.J Cell Sci.2005;118(Pt 7):1341-1353.
[7]Tasab M,Batten MR,Bulleid NJ.Hsp47:a molecular chaperone that interacts with and stabilizes correctly-folded procollagen.EMBO J.2000;19(10):2204-2211.
[8]Sauk JJ,Norris K,Hebert C,et al.Hsp47 binds to the KDEL receptor and cell surface expression is modulated by cytoplasmic and endosomal p H.Connect Tissue Res.1998;37(1-2):105-119.
[9]Ishikawa Y,B?chinger HP.A molecular ensemble in the r ER for procollagen maturation.Biochim Biophys Acta.2013;1833(11):2479-2491.
[10]Garnero P.Erratum to:The Role of Collagen Organization on the Properties of Bone.Calcif Tissue Int.2015;97(3):241.
[11]Cohen-Solal L,Zylberberg L,Sangalli A,et al.Substitution of an aspartic acid for glycine 700 in the alpha 2(I)chain of type Ⅰ collagen in a recurrent lethal type ⅠI osteogenesis imperfecta dramatically affects the mineralization of bone.J Biol Chem.1994;269(20):14751-14758.
[12]Bardai G,Lemyre E,Moffatt P,et al.Osteogenesis Imperfecta Type Ⅰ Caused by COL1A1 Deletions.Calcif Tissue Int.2016;98(1):76-84.
[13]Prockop DJ.Mutations that alter the primary structure of type Ⅰ collagen.The perils of a system for generating large structures by the principle of nucleated growth.J Biol Chem.1990;265(26):15349-15352.
[14]Gerhard DS,Wagner L,Feingold EA,et al.The status,quality,and expansion of the NIH full-length c DNA project:the Mammalian Gene Collection(MGC).Genome Res.2004;14(10B):2121-2127.
[15]He W,Wu WK,Wu YL,et al.Ginsenoside-Rg1 mediates microenvironment-dependent endothelial differentiation of human mesenchymal stem cells in vitro.J Asian Nat Prod Res.2011;13(1):1-11.
[16]Mizuno M,Fujisawa R,Kuboki Y.Type Ⅰ collagen-induced osteoblastic differentiation of bone-marrow cells mediated by collagen-alpha2beta1 integrin interaction.J Cell Physiol.2000;184(2):207-213.
[17]Bortell R,Barone LM,Tassinari MS,et al.Gene expression during endochondral bone development:evidence for coordinate expression of transforming growth factor beta 1and collagen type Ⅰ.J Cell Biochem.1990;44(2):81-91.
[18]Pittenger MF,Mackay AM,Beck SC,et al.Multilineage potential of adult human mesenchymal stem cells.Science.1999;284(5411):143-147.
[19]Aronow MA,Gerstenfeld LC,Owen TA,et al.Factors that promote progressive development of the osteoblast phenotype in cultured fetal rat calvaria cells.J Cell Physiol.1990;143(2):213-221.
[20]Hesse E,Hefferan TE,Tarara JE,et al.Collagen type Ⅰ hydrogel allows migration,proliferation,and osteogenic differentiation of rat bone marrow stromal cells.J Biomed Mater Res A.2010;94(2):442-449.
[21]Mizuno M,Kuboki Y.Osteoblast-related gene expression of bone marrow cells during the osteoblastic differentiation induced by type Ⅰ collagen.J Biochem.2001;129(1):133-138.
[22]Linsley C,Wu B,Tawil B.The effect of fibrinogen,collagen type Ⅰ,and fibronectin on mesenchymal stem cell growth and differentiation into osteoblasts.Tissue Eng Part A.2013;19(11-12):1416-1423.
[23]Salomon DS.Cell-cell and cell-extracellular matrix adhesion molecules communicate with growth factor receptors:an interactive signaling Web.Cancer Invest.2000;18(6):591-593.
[24]Staatz WD,Fok KF,Zutter MM,et al.Identification of a tetrapeptide recognition sequence for the alpha 2 beta 1integrin in collagen.J Biol Chem.1991;266(12):7363-7367.
[25]Puklin-Faucher E,Sheetz MP.The mechanical integrin cycle.J Cell Sci.2009;122(Pt 2):179-186.
[26]Schwartz MA.Integrins,oncogenes,and anchorage independence.J Cell Biol.1997;139(3):575-578.
[27]Wen LP,Fahrni JA,Troie S,et al.Cleavage of focal adhesion kinase by caspases during apoptosis.J Biol Chem.1997;272(41):26056-26061.
[28]Kim EK,Choi EJ.Pathological roles of MAPK signaling pathways in human diseases.Biochim Biophys Acta.2010;1802(4):396-405.
[29]Salasznyk RM,Klees RF,Williams WA,et al.Focal adhesion kinase signaling pathways regulate the osteogenic differentiation of human mesenchymal stem cells.Exp Cell Res.2007;313(1):22-37
[30]Jadlowiec J,Koch H,Zhang X,et al.Phosphophoryn regulates the gene expression and differentiation of NIH3T3,MC3T3-E1,and human mesenchymal stem cells via the integrin/MAPK signaling pathway.J Biol Chem.2004;279(51):53323-53330.
[31]Stein GS,Lian JB,Stein JL,et al.Transcriptional control of osteoblast growth and differentiation.Physiol Rev.1996;76(2):593-629.
[32]Ganta DR,Mc Carthy MB,Gronowicz GA.Ascorbic acid alters collagen integrins in bone culture.Endocrinology.1997;138(9):3606-3612.
[33]杨志明,屈艺.Ⅰ型胶原—整合素α2β1系统对成骨细胞生物学特性的调控[J].四川大学学报:医学版,2000,31(3):281-284.
[34]Wenstrup RJ,Witte DP,Florer JB.Abnormal differentiation in MC3T3-E1 preosteoblasts expressing a dominant-negative type Ⅰ collagen mutation.Connect Tissue Res.1996;35(1-4):249-257.
[35]Mofid MM,Manson PN,Robertson BC,et al.Craniofacial distraction osteogenesis:a review of 3278 cases.Plast Reconstr Surg.2001;108(5):1103-1114.
[36]Schreuder WH,Jansma J,Bierman MW,et al.Distraction osteogenesis versus bilateral sagittal split osteotomy for advancement of the retrognathic mandible:a review of the literature.Int J Oral Maxillofac Surg.2007;36(2):103-110.
[37]王大章,陈刚,胡静.牵张成骨在矫治牙颌面畸形中的应用[J].华西口腔医学杂志,1998,5(4):369-371.
[38]Welch RD,Lewis DD.Distraction osteogenesis.Vet Clin North Am Small Anim Pract.1999,29(5):1187-1205.
[39]柴本甫,汤雪明.实验性骨折愈合的细胞生物学[J].中华骨科杂志,1991,11(3):203-206.
[40]韦敏,穆雄铮,张涤生,等.颅面牵拉成骨胶原合成的研究[J].口腔颌面外科杂志,2001,11(1):32-34.
[41]丁宇翔,刘彦普,敖建华.牙槽突裂牵张成骨胶原合成的研究[J].实用口腔医学杂志,2005,21(4):477-479.
[42]商洪涛,刘锐,孙建壮,等.上颌骨缝牵张的组织学变化[J].中国组织工程研究,2007,11(10):1833-1836.
[43]Chen X,Li N,Lele Yang,et al.Expression of collagen I,collagen III and MMP-1 on the tension side of distracted tooth using periodontal ligament distraction osteogenesis in beagle dogs.Arch Oral Biol.2014;59(11):1217-1225.
[44]姜喜亮,朱晓文,胡静,等.整合素信号通路在大鼠骨髓间充质干细胞牵张中的作用和转导机制[J].中国口腔颌面外科杂志,2015,13(3):193-199.
[45]Liebschner MA.Biomechanical considerations of animal models used in tissue engineering of bone.Biomaterials.2004;25(9):1697-1714.
[46]Cisneros DA,Hung C,Franz CM,et al.Observing growth steps of collagen self-assembly by time-lapse high-resolution atomic force microscopy.J Struct Biol.2006;154(3):232-345.
[47]Olszta MJ,Cheng X,Sang SJ,et al.Bone structure and formation:A new perspective.Materials Science&Engineering R.2008;58(3):77-116.
[48]Xu Z,Yang Y,Zhao W,et al.Molecular mechanisms for intrafibrillar collagen mineralization in skeletal tissues.Biomaterials.2015;39:59-66.
[49]Wei Z,Huang ZL,Liao SS,et al.Nucleation Sites of Calcium Phosphate Crystals during Collagen Mineralization.Journal of the American Ceramic Society.2003;86(6):1052-1054.
[50]涂姜磊,郭富强,吕春春,等.胶原诱导沉积类骨HA及其机制研究[J].生物医学工程学杂志,2011,28(1):99-103.
[51]Nudelman F,Pieterse K,George A,et al.The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors.Nat Mater.2010;9(12):1004-1009.
[52]Cantaert B,Kim YY,Ludwig H,et al.Think Positive:Phase Separation Enables a Positively Charged Additive to Induce Dramatic Changes in Calcium Carbonate Morphology.Advanced Functional Materials.2012;22(5):907-915.
[53]Zurick KM,Qin C,Bernards MT.Mineralization induction effects of osteopontin,bone sialoprotein,and dentin phosphoprotein on a biomimetic collagen substrate.J Biomed Mater Res A.2013;101(6):1571-1581.
[54]Qiu ZY,Cui Y,Tao CS,et al.Mineralized Collagen:Rationale,Current Status,and Clinical Applications.Materials(Basel).2015;8(8):4733-4750.
[55]Kerns JG,Buckley K,Churchwell J,et al.Is the Collagen Primed for Mineralization in Specific Regions of the Turkey Tendon?An Investigation of the Protein-Mineral Interface Using Raman Spectroscopy.Anal Chem.2016;88(3):1559-1563.
[56]Wang Y,Aza?s T,Robin M,et al.The predominant role of collagen in the nucleation,growth,structure and orientation of bone apatite.Nat Mater.2012;11(8):724-733.
[57]Hvistendahl M.China's push in tissue engineering.Science.2012;338(6109):900-902.
[58]Kumar MS,Kirubanandan S,Sripriya R,et al.Triphala incorporated collagen sponge--a smart biomaterial for infected dermal wound healing.J Surg Res.2010;158(1):162-170.