Issue
Evolutionary analysis of TSP-1 gene in Plateau zokor (MyospalaxBaileyi) and its expression pattern under hypoxia
Corresponding Author(s) : Dengbang Wei
Cellular and Molecular Biology,
Vol. 65 No. 3: Issue 3
Abstract
The plateau zokor (Myospalaxbaileyi) is a specialized subterranean rodent that lives on the Qinghai-Tibet Plateau, and has successfully adapted to hypoxic environment. Raised expression of vascular endothelial growth factor (VEGF) and enhanced microvessel density (MVD) in tissues enable subterranean rodents to adapt to hypoxic sealed burrows. However, the expression of VEGF is inhibited by decreases in oxygen content, which is different from what obtains in Sprague Dawley (SD)rats. Thromspondin-1(TSP-1) is the first endogenous angiogenesis inhibitor identified inp53 pathway. It has several domains that bind to different proteins which regulate cell-to-cell interactions, inhibit endothelial cell proliferation and induce endothelial cell apoptosis (anti-angiogenesis). In this study, we analyzed the coding region and the expression pattern of TSP-1 gene in plateau zokor under different oxygen partial pressures using bioinformatics and qRT-PCR, respectively. Our results showed that the base and amino acid homologies between plateau zokor and Northern Israeli blind subterranean mole rat (Nannospalaxgalili) were 95.08 and 97.61%, respectively. There were eight parallel evolution sites with Nannospalaxgalili. Evaluation by ‘Sorting Tolerant From Intolerant' (SIFT) algorithm showed four sites with significant effects on the function of TSP-1. Three-dimensional (3D) structures revealed that Asp185 and Thr270 were located in the NH2 terminal domain, with Glu536 in the Type I repeat domain, and Thr1092 in the COOH terminal domain. Compared to SD rats, the polarities of these four mutation sites changed. The expression levels of TSP-1 in plateau zokor tissues increased significantly from 2 260 m(16.12kPa) to 3 300 m(14.13kPa), but there was no significant difference in TSP-1 expression in SD rats. In conclusion, due to long-term adaption to the hypoxic environment of sealed burrows, plateau zokor upregulates the expression of TSP-1 to effect anti-angiogenesis. Moreover, mutations in gene structure of TSP-1 may play an important role in inhibiting angiogenesis.
Keywords
Download Citation
Endnote/Zotero/Mendeley (RIS)BibTeX
- Heidenreich R, Rocken M, Ghoreschi K. Angiogenesis drives psoriasis pathogenesis. Int J Exp Pathol 2009; 90: 232-248.
- Shweiki D, Itin A, Soffer D, Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nat 1992; 359: 843-845.
- Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 1996; 16: 4604-4613.
- Ravi R, Mookerjee B, Bhujwalla ZM, Sutter CH, Artemov D, Zeng Q, et al. Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1alpha. Genes Dev 2000; 14: 34-44.
- Liao D, Johnson RS. Hypoxia: A key regulator of angiogenesis in cancer. Cancer Metastasis Rev 2007; 26: 281-290.
- Teodoro JG, Evans SK, Green MR. Inhibition of tumor angiogenesis by p53: a new role for the guardian of the genome. J Mol Med 2007; 85: 1175-1186.
- Paul B. Thrombospondins function as regulators of angiogenesis. J Cell Commun Signal 2009; 3: 189-200.
- Silverstein RL. The face of TSR revealed: an extracellular signaling domain is exposed. J Cell Biol 2002; 159: 203-206.
- Bornstein P. Thrombospondins function as regulators of angiogenesis. J Cell Commun Signal 2009; 3: 189-200.
- Maloney JP, Stearman RS, Bull TM, Calabrese DW, Tripp-Addison ML, Wick MJ, et al. Loss-of-function thrombospondin-1 mutations in familial pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 2012; 302: 541-554.
- Phelan MW, Forman LW, Perrine SP, Faller DV. Hypoxia increases thrombospondin-1 transcript and protein in cultured endothelial cells. J Lab Clin Med 1998; 132: 519-529.
- Fontana A, Fileur S, Guglielmi J, Frappart L, Bruno-Bossio G, Boissier S, et al. Human breast tumors override the antiangiogenic effect of stromal thrombospondin-1 in vivo. Int J Cancer 2005; 116: 686-691.
- Takahashi M, Oka M, Ikeda T, Akiba S, Sato T. Role of thrombospondin-1 in hypoxia-induced migration of human vascular smooth muscle cells. Yakugaku Zasshi J Pharm 2008; 128: 377-383.
- Morgan RL, Nikitorowicz J, Shiwen X, Leask A, Tsui J, Abraham D, et al. Thrombospondin 1 in hypoxia-conditioned media blocks the growth of human microvascular endothelial cells and is increased in systemic sclerosis tissues. Fibrogenesis Tissue Repair 2011; 4: 13.
- Fan NC, Shi YZ. Taxonomy of Chinese zokor (Eospalax) subgenus. Acta Theriologica Sinica 1982; 2: 183-199.
- Wei DB, Wei L, Zhang JM, Yu HY. Blood-gas properties of plateau zokor (Myospalax baileyi). Comp Biochem Physiol 2006; 145: 372-375.
- Zheng YN, Zhu RJ, Wang DW, Wei L, Wei DB. Gene coding and mRNA expression of vascular endothelial growth factor as well as microvessel density in brain of plateau zokor: comparison with other rodents. Acta Physiologica Sinica 2011; 63: 155-163.
- Vleck D. Burrow structure and foraging costs in the fossorial rodent, Thomomys bottae. Oecologia 1981; 49: 391-396.
- Nevo E. Mosaic evolution of subterranean mammals: regression, progression and global convergence. Oxford University Press, Oxford. 1999.
- Wei DB, Wei L. The Mensuration Results of the Number of Red Cell, the Density of Hemoglobin and the Contents of Myoglobin in Plateau Zokor. J Qinghai Univ 2001; 19: 1-2.
- Avivi A, Resnick MB, Nevo E, Joel A, Levy AP. Adaptive hypoxic tolerance in subterranean mole rat Spalax ehrenbergi: the role of vascular endothelial growth factor. FEBS Lett 1999; 452: 133-140.
- Burland TG. DNASTAR's Lasergene sequence analysis software. Methods Mol Biol 2000; 132: 71-91.
- Kumar S, Stecher G, Tamura K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33: 1870-1874.
- Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinform 2001; 17: 754-755.
- Gamerman D, Lopes HF. Markov chain Monte Carlo: stochastic simulation for Bayesian inference. Boca Raton: CRC Press. 2006.
- Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012; 9: 772-772.
- Yamaoka K, Nakagawa T, Uno T. Application of Akaike's information criterion (AIC) in the evaluation of linear pharmacokinetic equations. J Pharmacokinet Biopharm 1978; 6: 165-175.
- Sakamoto Y, Ishiguro M, Kitagawa G. Akaike information criterion statistics. Dordrecht, The Netherlands: D. Reidel, 81.1986.
- Bozdogan H. Model selection and Akaike's information criterion (AIC): The general theory and its analytical extensions. Psychometrika 1987; 52: 345-370.
- Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007; 24: 1586-1591.
- Zhang J, Nielsen R, Yang Z. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 2005; 22: 2472-2479.
- Wang Z, Xu S, Du K, Huang F, Chen Z, Zhou K, et al. Evolution of digestive enzymes and RNASE1 provides insights into dietary switch of cetaceans. Mol Biol Evol 2016; 33: 3144-3157.
- Nei M, Kumar S. Molecular evolution and phylogenetics. Oxford university press. 2000.
- Zhang J, Kumar S. Detection of convergent and parallel evolution at the amino acid sequence level. Mol Biol Evol 1997; 14: 527-536.
- Kumar P, Henikoff S, Ng PC. Predicting the effects of coding non-synonymous variants on protein function using the sift algorithm. Nat Protoc 2009; 4: 1073-1081.
- Arnold K, Bordoli L, Kopp J, Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bio informatics 2006; 22: 195-201.
- Schrodinger LLC. The PYMOL molecular graphics system, Version 1.4.1. 2010.
- Niesters HG. Quantitation of viral load using real-time amplification techniques. Methods 2001; 25: 419-429.
- Zeng J, Wang Z, Shi Z. Metabolic characteristics and some physiological parameters of the mole rat (Myospalax baileyi) in an alpine area. Acta Biol Plat Sin 1984; 3: 163-171.
- Shao Y, Li JX, Ge RL, Zhong L, Irwin DM, Murphy RW, et al. Genetic adaptions of the plateau zokor in high-elevation burrows. Sci Rep UK 2015; 5: 17262.
- Wilson DE,Reeder DM. Mammal Species of the World: A Taxonomic and Geographic Reference (3rd Ed), Johns Hopkins University Press, 2005.
- Nevo E, Ivanitskaya E, Beiles A. Adaptive radiation of blind subterranean mole rats: naming and revisiting the four sibling species of the Spalax ehrenbergi superspecies in Israel: Spalax galili (2n=52), S. golani (2n=54), S. carmeli (2n=58), and S. judaei (2n=60). Backhuys Publishers, Leiden. 2001.
- Shams I, Avivi A, Nevo E. Oxygen and carbon dioxide fluctuations in burrows of subterranean blind mole rats indicate tolerance to hypoxic–hypercapnic stresses. CompBiochemPhys A 2005; 142: 376-382.
- Wei DB, Wang DW, Wei L, Ma BY. Differences in Physiological Adaptive Strategies to Hypoxic Environments in Plateau Zokor and Plateau Pika. High Alt Med 2012; 36: 1.
- Gurnett AM, O'Connell JP, Harris DE, Lehmann H, Joysey KA, Nevo E. The myoglobin of rodents:Lagostomus maximus (viscacha) and Spalax ehrenbergi (mole rat). J Prot Chem 1984; 3: 445-454.
- Kleinschmidt T, Nevo E, Goodman M, Braunitzer G. Mole rat hemoglobin: primary structure and evolutionary aspects in a second karyotype of Spalax ehrenbergi, Rodentia, (2n=52). Biol Chem Hoppe Seyler 1985; 366: 679-685.
- Widmer HR, Hoppeler H, Nevo E, Richard TC, Weibel ER. Working underground: Respiratory adaptations in the blind mole rat. Proc Natl Acad Sci USA 1997; 94: 2062-2067.
- Howell K, Ooi H, Preston R, Mcloughlin P. Structural basis of hypoxic pulmonary hypertension: the modifying effect of chronic hypercapnia. Exp Physiol 2004; 89: 66-72.
- Yang ZY, Zhang Y, Chen LN. Single amino acid changes in naked mole rat may reveal new anti-cancer mechanisms in mammals. Gene 2015; 572: 101-107.
- Kazerounian S, Yee KO, Lawler J. Thrombospondins in cancer. Cell Mol Life Sci 2008; 65: 700-712.
- Clezardin P, Frappart L, Clerget M, Pechoux C, Delmas PD. Expression of thrombospondin (TSP1) and its receptors (CD36 and CD51) in normal, hyperplastic, and neoplastic human breast. Cancer Res 1993; 53: 1421-1430.
- Zhao Y, Ren JL, Wang MY, Zhang ST, Liu Y, Li M, et al. Codon 104 variation of p53 gene provides adaptive apoptotic response to extreme environments in mammals of the Tibet plateau. P Natl Acad Sci USA 2013; 110: 20639-20644.
- An ZF, Zhao K, Wei LN, Wang ZJ, Li SH, Wei L, et al. p53 gene cloning and response to hypoxia in the plateau zokor, Myospalax baileyi. Animal Biol 2018; 12: 3.
- Chen H, Sottile J, Strickland DK, Mosher DF. Binding and degradation of thrombospondin-1 mediated through heparan sulphate proteoglycans and low-density-lipoprotein receptor-related protein: localization of the functional activity to the trimeric N-terminal heparin-binding region of thrombospondin-1. Biochem J 1996; 318: 959-963.
- Yang Z, Strickland DK, Bornstein P. Extracellular matrix metalloproteinase 2 levels are regulated by the low density lipoprotein related scavenger receptor and thrombospondin 2. J Biol Chem 2001; 276: 8403-8408.
- Hahn-Dantona E, Ruiz JF, Bornstein P, Strickland DK. The low density lipoprotein receptor-related protein modulates levels of matrix metalloproteinase 9 (MMP-9) by mediating its cellular catabolism. J Biol Chem 2001; 276: 15498-15503.
- Greenaway J, Moorehead RP, Bornstein P, Lawler J, LaMarre J, Petrik J. Thrombospondin-1 inhibits VEGF levels in the ovary directly by binding and internalization via the low density lipoprotein receptor-related protein-1 (LRP-1). J Cell Physiol 2007; 210: 807-818.
- Febbraio M, Hajjar DP, Silverstein RL. CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation and lipid metabolism. J Clin Invest 2001; 108: 785-791.
- Yasuyoshi M, Shin-ichi W, Hiroshi K, Hideki S. Thrombospondin-1- derived 4N1K peptide expression is negatively associated with malignant aggressiveness and prognosis in urothelial carcinoma of the upper urinary tract. BMC Cancer 2012; 12: 2-9.
- Goldshmidt O, Zcharia E, Abramovitch R, Metzger S, Aingorn H, Friedmann Y, et al. Cell surface expression and secretion of heparanase markedly promote tumor angiogenesis and metastasis. Proc Natl Acad Sci USA 2002; 99: 10031-10036.
- Luke MR, Joanna N, Xu SW, Andrew L, Janice T, David A, et al. Thrombospondin 1 in hypoxia-conditioned media blocks the growth of human microvascular endothelial cells and is increased in systemic sclerosis tissues. Fibrogenesis Tissue Repair 2011; 4: 13.
- Good DJ, Polverini PJ, Rastinejad F, Le Beau MM, Lemons RS, Frazier WA, et al. A tumor suppressor-dependent inhibitor of angiogenesis is immunologically and functionally indistinguishable from a fragment of thrombospondin. Proc Natl Acad Sci USA 1990; 87: 6624-6662.
- Dameron KM, Volpert OV, Tainsky MA, Bouck N. Control of angiogenesis in fibroblasts by p53 regulation of thromspondin-1. Sci 1994; 21: 1582-1584.
- Lawler J, Miao W M, Duquette M. Thrombospondin-1 gene expression affects survival and tumor spectrum of p53-deficient mice. Am J Pathol 2001; 159: 1949-1956.
- Wang MY, Zhao Y, Zhang ST, Chen XQ, Du JZ. The regulation of expression for p53 and its target genes in simulate hypoxia. China J Appl Physiol 2013; 29: 136-138.
References
Heidenreich R, Rocken M, Ghoreschi K. Angiogenesis drives psoriasis pathogenesis. Int J Exp Pathol 2009; 90: 232-248.
Shweiki D, Itin A, Soffer D, Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nat 1992; 359: 843-845.
Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 1996; 16: 4604-4613.
Ravi R, Mookerjee B, Bhujwalla ZM, Sutter CH, Artemov D, Zeng Q, et al. Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1alpha. Genes Dev 2000; 14: 34-44.
Liao D, Johnson RS. Hypoxia: A key regulator of angiogenesis in cancer. Cancer Metastasis Rev 2007; 26: 281-290.
Teodoro JG, Evans SK, Green MR. Inhibition of tumor angiogenesis by p53: a new role for the guardian of the genome. J Mol Med 2007; 85: 1175-1186.
Paul B. Thrombospondins function as regulators of angiogenesis. J Cell Commun Signal 2009; 3: 189-200.
Silverstein RL. The face of TSR revealed: an extracellular signaling domain is exposed. J Cell Biol 2002; 159: 203-206.
Bornstein P. Thrombospondins function as regulators of angiogenesis. J Cell Commun Signal 2009; 3: 189-200.
Maloney JP, Stearman RS, Bull TM, Calabrese DW, Tripp-Addison ML, Wick MJ, et al. Loss-of-function thrombospondin-1 mutations in familial pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 2012; 302: 541-554.
Phelan MW, Forman LW, Perrine SP, Faller DV. Hypoxia increases thrombospondin-1 transcript and protein in cultured endothelial cells. J Lab Clin Med 1998; 132: 519-529.
Fontana A, Fileur S, Guglielmi J, Frappart L, Bruno-Bossio G, Boissier S, et al. Human breast tumors override the antiangiogenic effect of stromal thrombospondin-1 in vivo. Int J Cancer 2005; 116: 686-691.
Takahashi M, Oka M, Ikeda T, Akiba S, Sato T. Role of thrombospondin-1 in hypoxia-induced migration of human vascular smooth muscle cells. Yakugaku Zasshi J Pharm 2008; 128: 377-383.
Morgan RL, Nikitorowicz J, Shiwen X, Leask A, Tsui J, Abraham D, et al. Thrombospondin 1 in hypoxia-conditioned media blocks the growth of human microvascular endothelial cells and is increased in systemic sclerosis tissues. Fibrogenesis Tissue Repair 2011; 4: 13.
Fan NC, Shi YZ. Taxonomy of Chinese zokor (Eospalax) subgenus. Acta Theriologica Sinica 1982; 2: 183-199.
Wei DB, Wei L, Zhang JM, Yu HY. Blood-gas properties of plateau zokor (Myospalax baileyi). Comp Biochem Physiol 2006; 145: 372-375.
Zheng YN, Zhu RJ, Wang DW, Wei L, Wei DB. Gene coding and mRNA expression of vascular endothelial growth factor as well as microvessel density in brain of plateau zokor: comparison with other rodents. Acta Physiologica Sinica 2011; 63: 155-163.
Vleck D. Burrow structure and foraging costs in the fossorial rodent, Thomomys bottae. Oecologia 1981; 49: 391-396.
Nevo E. Mosaic evolution of subterranean mammals: regression, progression and global convergence. Oxford University Press, Oxford. 1999.
Wei DB, Wei L. The Mensuration Results of the Number of Red Cell, the Density of Hemoglobin and the Contents of Myoglobin in Plateau Zokor. J Qinghai Univ 2001; 19: 1-2.
Avivi A, Resnick MB, Nevo E, Joel A, Levy AP. Adaptive hypoxic tolerance in subterranean mole rat Spalax ehrenbergi: the role of vascular endothelial growth factor. FEBS Lett 1999; 452: 133-140.
Burland TG. DNASTAR's Lasergene sequence analysis software. Methods Mol Biol 2000; 132: 71-91.
Kumar S, Stecher G, Tamura K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33: 1870-1874.
Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinform 2001; 17: 754-755.
Gamerman D, Lopes HF. Markov chain Monte Carlo: stochastic simulation for Bayesian inference. Boca Raton: CRC Press. 2006.
Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012; 9: 772-772.
Yamaoka K, Nakagawa T, Uno T. Application of Akaike's information criterion (AIC) in the evaluation of linear pharmacokinetic equations. J Pharmacokinet Biopharm 1978; 6: 165-175.
Sakamoto Y, Ishiguro M, Kitagawa G. Akaike information criterion statistics. Dordrecht, The Netherlands: D. Reidel, 81.1986.
Bozdogan H. Model selection and Akaike's information criterion (AIC): The general theory and its analytical extensions. Psychometrika 1987; 52: 345-370.
Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007; 24: 1586-1591.
Zhang J, Nielsen R, Yang Z. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 2005; 22: 2472-2479.
Wang Z, Xu S, Du K, Huang F, Chen Z, Zhou K, et al. Evolution of digestive enzymes and RNASE1 provides insights into dietary switch of cetaceans. Mol Biol Evol 2016; 33: 3144-3157.
Nei M, Kumar S. Molecular evolution and phylogenetics. Oxford university press. 2000.
Zhang J, Kumar S. Detection of convergent and parallel evolution at the amino acid sequence level. Mol Biol Evol 1997; 14: 527-536.
Kumar P, Henikoff S, Ng PC. Predicting the effects of coding non-synonymous variants on protein function using the sift algorithm. Nat Protoc 2009; 4: 1073-1081.
Arnold K, Bordoli L, Kopp J, Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bio informatics 2006; 22: 195-201.
Schrodinger LLC. The PYMOL molecular graphics system, Version 1.4.1. 2010.
Niesters HG. Quantitation of viral load using real-time amplification techniques. Methods 2001; 25: 419-429.
Zeng J, Wang Z, Shi Z. Metabolic characteristics and some physiological parameters of the mole rat (Myospalax baileyi) in an alpine area. Acta Biol Plat Sin 1984; 3: 163-171.
Shao Y, Li JX, Ge RL, Zhong L, Irwin DM, Murphy RW, et al. Genetic adaptions of the plateau zokor in high-elevation burrows. Sci Rep UK 2015; 5: 17262.
Wilson DE,Reeder DM. Mammal Species of the World: A Taxonomic and Geographic Reference (3rd Ed), Johns Hopkins University Press, 2005.
Nevo E, Ivanitskaya E, Beiles A. Adaptive radiation of blind subterranean mole rats: naming and revisiting the four sibling species of the Spalax ehrenbergi superspecies in Israel: Spalax galili (2n=52), S. golani (2n=54), S. carmeli (2n=58), and S. judaei (2n=60). Backhuys Publishers, Leiden. 2001.
Shams I, Avivi A, Nevo E. Oxygen and carbon dioxide fluctuations in burrows of subterranean blind mole rats indicate tolerance to hypoxic–hypercapnic stresses. CompBiochemPhys A 2005; 142: 376-382.
Wei DB, Wang DW, Wei L, Ma BY. Differences in Physiological Adaptive Strategies to Hypoxic Environments in Plateau Zokor and Plateau Pika. High Alt Med 2012; 36: 1.
Gurnett AM, O'Connell JP, Harris DE, Lehmann H, Joysey KA, Nevo E. The myoglobin of rodents:Lagostomus maximus (viscacha) and Spalax ehrenbergi (mole rat). J Prot Chem 1984; 3: 445-454.
Kleinschmidt T, Nevo E, Goodman M, Braunitzer G. Mole rat hemoglobin: primary structure and evolutionary aspects in a second karyotype of Spalax ehrenbergi, Rodentia, (2n=52). Biol Chem Hoppe Seyler 1985; 366: 679-685.
Widmer HR, Hoppeler H, Nevo E, Richard TC, Weibel ER. Working underground: Respiratory adaptations in the blind mole rat. Proc Natl Acad Sci USA 1997; 94: 2062-2067.
Howell K, Ooi H, Preston R, Mcloughlin P. Structural basis of hypoxic pulmonary hypertension: the modifying effect of chronic hypercapnia. Exp Physiol 2004; 89: 66-72.
Yang ZY, Zhang Y, Chen LN. Single amino acid changes in naked mole rat may reveal new anti-cancer mechanisms in mammals. Gene 2015; 572: 101-107.
Kazerounian S, Yee KO, Lawler J. Thrombospondins in cancer. Cell Mol Life Sci 2008; 65: 700-712.
Clezardin P, Frappart L, Clerget M, Pechoux C, Delmas PD. Expression of thrombospondin (TSP1) and its receptors (CD36 and CD51) in normal, hyperplastic, and neoplastic human breast. Cancer Res 1993; 53: 1421-1430.
Zhao Y, Ren JL, Wang MY, Zhang ST, Liu Y, Li M, et al. Codon 104 variation of p53 gene provides adaptive apoptotic response to extreme environments in mammals of the Tibet plateau. P Natl Acad Sci USA 2013; 110: 20639-20644.
An ZF, Zhao K, Wei LN, Wang ZJ, Li SH, Wei L, et al. p53 gene cloning and response to hypoxia in the plateau zokor, Myospalax baileyi. Animal Biol 2018; 12: 3.
Chen H, Sottile J, Strickland DK, Mosher DF. Binding and degradation of thrombospondin-1 mediated through heparan sulphate proteoglycans and low-density-lipoprotein receptor-related protein: localization of the functional activity to the trimeric N-terminal heparin-binding region of thrombospondin-1. Biochem J 1996; 318: 959-963.
Yang Z, Strickland DK, Bornstein P. Extracellular matrix metalloproteinase 2 levels are regulated by the low density lipoprotein related scavenger receptor and thrombospondin 2. J Biol Chem 2001; 276: 8403-8408.
Hahn-Dantona E, Ruiz JF, Bornstein P, Strickland DK. The low density lipoprotein receptor-related protein modulates levels of matrix metalloproteinase 9 (MMP-9) by mediating its cellular catabolism. J Biol Chem 2001; 276: 15498-15503.
Greenaway J, Moorehead RP, Bornstein P, Lawler J, LaMarre J, Petrik J. Thrombospondin-1 inhibits VEGF levels in the ovary directly by binding and internalization via the low density lipoprotein receptor-related protein-1 (LRP-1). J Cell Physiol 2007; 210: 807-818.
Febbraio M, Hajjar DP, Silverstein RL. CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation and lipid metabolism. J Clin Invest 2001; 108: 785-791.
Yasuyoshi M, Shin-ichi W, Hiroshi K, Hideki S. Thrombospondin-1- derived 4N1K peptide expression is negatively associated with malignant aggressiveness and prognosis in urothelial carcinoma of the upper urinary tract. BMC Cancer 2012; 12: 2-9.
Goldshmidt O, Zcharia E, Abramovitch R, Metzger S, Aingorn H, Friedmann Y, et al. Cell surface expression and secretion of heparanase markedly promote tumor angiogenesis and metastasis. Proc Natl Acad Sci USA 2002; 99: 10031-10036.
Luke MR, Joanna N, Xu SW, Andrew L, Janice T, David A, et al. Thrombospondin 1 in hypoxia-conditioned media blocks the growth of human microvascular endothelial cells and is increased in systemic sclerosis tissues. Fibrogenesis Tissue Repair 2011; 4: 13.
Good DJ, Polverini PJ, Rastinejad F, Le Beau MM, Lemons RS, Frazier WA, et al. A tumor suppressor-dependent inhibitor of angiogenesis is immunologically and functionally indistinguishable from a fragment of thrombospondin. Proc Natl Acad Sci USA 1990; 87: 6624-6662.
Dameron KM, Volpert OV, Tainsky MA, Bouck N. Control of angiogenesis in fibroblasts by p53 regulation of thromspondin-1. Sci 1994; 21: 1582-1584.
Lawler J, Miao W M, Duquette M. Thrombospondin-1 gene expression affects survival and tumor spectrum of p53-deficient mice. Am J Pathol 2001; 159: 1949-1956.
Wang MY, Zhao Y, Zhang ST, Chen XQ, Du JZ. The regulation of expression for p53 and its target genes in simulate hypoxia. China J Appl Physiol 2013; 29: 136-138.