Ribonuclease 4 protects neuron degeneration by promoting angiogenesis, neurogenesis, and neuronal survival under stress
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  • 作者:Shuping Li (1) (2)
    Jinghao Sheng (1) (3)
    Jamie K. Hu (1)
    Wenhao Yu (1)
    Hiroko Kishikawa (1)
    Miaofen G. Hu (1)
    Kaori Shima (4)
    David Wu (5)
    Zhengping Xu (3)
    Winnie Xin (6)
    Katherine B. Sims (6)
    John E. Landers (7)
    Robert H. Brown Jr. (7)
    Guo-fu Hu (1)
  • 关键词:Ribonuclease 4 ; Angiogenin ; Angiogenesis ; Neurogenesis ; Neuroprotection ; Amyotrophic lateral sclerosis (ALS)
  • 刊名:Angiogenesis
  • 出版年:2013
  • 出版时间:April 2013
  • 年:2013
  • 卷:16
  • 期:2
  • 页码:387-404
  • 全文大小:1476KB
  • 参考文献:1. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860鈥?21 CrossRef
    2. Cho S, Beintema JJ, Zhang J (2005) The ribonuclease A superfamily of mammals and birds: identifying new members and tracing evolutionary histories. Genomics 85:208鈥?20 CrossRef
    3. Cho S, Zhang J (2007) Zebrafish ribonucleases are bactericidal: implications for the origin of the vertebrate RNase A superfamily. Mol Biol Evol 24:1259鈥?268 CrossRef
    4. Rosenberg HF, Tenen DG, Ackerman SJ (1989) Molecular cloning of the human eosinophil-derived neurotoxin: a member of the ribonuclease gene family. Proc Natl Acad Sci USA 86:4460鈥?464 CrossRef
    5. Barker RL, Loegering DA, Ten RM, Hamann KJ, Pease LR, Gleich GJ (1989) Eosinophil cationic protein cDNA. Comparison with other toxic cationic proteins and ribonucleases. J Immunol 143:952鈥?55
    6. Fredens K, Dahl R, Venge P (1982) The Gordon phenomenon induced by the eosinophil cationic protein and eosinophil protein X. J Allergy Clin Immunol 70:361鈥?66 CrossRef
    7. Yang D, Chen Q, Rosenberg HF, Rybak SM, Newton DL, Wang ZY, Fu Q, Tchernev VT, Wang M, Schweitzer B et al (2004) Human ribonuclease A superfamily members, eosinophil-derived neurotoxin and pancreatic ribonuclease, induce dendritic cell maturation and activation. J Immunol 173:6134鈥?142
    8. Hamann KJ, Barker RL, Loegering DA, Gleich GJ (1987) Comparative toxicity of purified human eosinophil granule proteins for newborn larvae of Trichinella spiralis. J Parasitol 73:523鈥?29 CrossRef
    9. Lehrer RI, Szklarek D, Barton A, Ganz T, Hamann KJ, Gleich GJ (1989) Antibacterial properties of eosinophil major basic protein and eosinophil cationic protein. J Immunol 142:4428鈥?434
    10. Rosenberg HF, Domachowske JB (2001) Eosinophils, eosinophil ribonucleases, and their role in host defense against respiratory virus pathogens. J Leukoc Biol 70:691鈥?98
    11. Fett JW, Strydom DJ, Lobb RR, Alderman EM, Bethune JL, Riordan JF, Vallee BL (1985) Isolation and characterization of angiogenin, an angiogenic protein from human carcinoma cells. Biochemistry 24:5480鈥?486 CrossRef
    12. Li S, Hu GF (2010) Angiogenin-mediated rRNA transcription in cancer and neurodegeneration. Int J Biochem Mol Biol 1:26鈥?5
    13. Xu ZP, Tsuji T, Riordan JF, Hu GF (2002) The nuclear function of angiogenin in endothelial cells is related to rRNA production. Biochem Biophys Res Commun 294:287鈥?92 CrossRef
    14. Xu ZP, Tsuji T, Riordan JF, Hu GF (2003) Identification and characterization of an angiogenin-binding DNA sequence that stimulates luciferase reporter gene expression. Biochemistry 42:121鈥?28 CrossRef
    15. Yoshioka N, Wang L, Kishimoto K, Tsuji T, Hu GF (2006) A therapeutic target for prostate cancer based on angiogenin-stimulated angiogenesis and cancer cell proliferation. Proc Natl Acad Sci USA 103:14519鈥?4524 CrossRef
    16. Emara MM, Ivanov P, Hickman T, Dawra N, Tisdale S, Kedersha N, Hu GF, Anderson P (2010) Angiogenin-induced tRNA-derived stress-induced RNAs promote stress-induced stress granule assembly. J Biol Chem 285:10959鈥?0968 CrossRef
    17. Yamasaki S, Ivanov P, Hu GF, Anderson P (2009) Angiogenin cleaves tRNA and promotes stress-induced translational repression. J Cell Biol 185:35鈥?2 CrossRef
    18. Ivanov P, Emara MM, Villen J, Gygi SP, Anderson P (2011) Angiogenin-Induced tRNA Fragments Inhibit Translation Initiation. Mol Cell 43:613鈥?23 CrossRef
    19. Thompson DM, Lu C, Green PJ, Parker R (2008) tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA 14:2095鈥?103 CrossRef
    20. Hofsteenge J, Vicentini A, Zelenko O (1998) Ribonuclease 4, an evolutionarily highly conserved member of the superfamily. Cell Mol Life Sci 54:804鈥?10 CrossRef
    21. Shapiro R, Fett JW, Strydom DJ, Vallee BL (1986) Isolation and characterization of a human colon carcinoma-secreted enzyme with pancreatic ribonuclease-like activity. Biochemistry 25:7255鈥?264 CrossRef
    22. Dyer KD, Rosenberg HF (2005) The mouse RNase 4 and RNase 5/ang 1 locus utilizes dual promoters for tissue-specific expression. Nucleic Acids Res 33:1077鈥?086 CrossRef
    23. Futami J, Tsushima Y, Murato Y, Tada H, Sasaki J, Seno M, Yamada H (1997) Tissue-specific expression of pancreatic-type RNases and RNase inhibitor in humans. DNA Cell Biol 16:413鈥?19 CrossRef
    24. Strydom DJ (1998) The angiogenins. Cell Mol Life Sci 54:811鈥?24 CrossRef
    25. Greenway MJ, Andersen PM, Russ C, Ennis S, Cashman S, Donaghy C, Patterson V, Swingler R, Kieran D, Prehn J et al (2006) ANG mutations segregate with familial and 鈥榮poradic鈥?amyotrophic lateral sclerosis. Nat Genet 38:411鈥?13 CrossRef
    26. Wu D, Yu W, Kishikawa H, Folkerth RD, Iafrate AJ, Shen Y, Xin W, Sims K, Hu GF (2007) Angiogenin loss-of-function mutations in amyotrophic lateral sclerosis. Ann Neurol 62:609鈥?17 CrossRef
    27. Kieran D, Sebastia J, Greenway MJ, King MA, Connaughton D, Concannon CG, Fenner B, Hardiman O, Prehn JH (2008) Control of motoneuron survival by angiogenin. J Neurosci 28:14056鈥?4061 CrossRef
    28. Subramanian V, Feng Y (2007) A new role for angiogenin in neurite growth and pathfinding: implications for amyotrophic lateral sclerosis. Hum Mol Genet 16:1445鈥?453 CrossRef
    29. Baumer D, Ansorge O, Almeida M, Talbot K (2010) The role of RNA processing in the pathogenesis of motor neuron degeneration. Expert Rev Mol Med 12:e21 CrossRef
    30. van Blitterswijk M, Landers JE (2010) RNA processing pathways in amyotrophic lateral sclerosis. Neurogenetics 11:275鈥?90 CrossRef
    31. Strong MJ (2010) The evidence for altered RNA metabolism in amyotrophic lateral sclerosis (ALS). J Neurol Sci 288:1鈥?2 CrossRef
    32. Holloway DE, Hares MC, Shapiro R, Subramanian V, Acharya KR (2001) High-level expression of three members of the murine angiogenin family in Escherichia coli and purification of the recombinant proteins. Protein Expr Purif 22:307鈥?17 CrossRef
    33. Shapiro R, Weremowicz S, Riordan JF, Vallee BL (1987) Ribonucleolytic activity of angiogenin: essential histidine, lysine, and arginine residues. Proc Natl Acad Sci USA 84:8783鈥?787 CrossRef
    34. Bibel M, Richter J, Lacroix E, Barde YA (2007) Generation of a defined and uniform population of CNS progenitors and neurons from mouse embryonic stem cells. Nat Protoc 2:1034鈥?043 CrossRef
    35. Shapiro R, Fox EA, Riordan JF (1989) Role of lysines in human angiogenin: chemical modification and site-directed mutagenesis. Biochemistry 28:1726鈥?732 CrossRef
    36. Messmore JM, Fuchs DN, Raines RT (1995) Ribonuclease a: revealing structure-function relationships with semisynthesis. J Am Chem Soc 117:8057鈥?060 CrossRef
    37. Di Liddo R, Dalzoppo D, Baiguera S, Conconi MT, Dettin M, Parnigotto PP, Grandi C (2010) In vitro biological activity of bovine milk ribonuclease-4. Mol Med Report 3:127鈥?32
    38. Donovan D, Brown NJ, Bishop ET, Lewis CE (2001) Comparison of three in vitro human 鈥榓ngiogenesis鈥?assays with capillaries formed in vivo. Angiogenesis 4:113鈥?21 CrossRef
    39. Masson VV, Devy L, Grignet-Debrus C, Bernt S, Bajou K, Blacher S, Roland G, Chang Y, Fong T, Carmeliet P et al (2002) Mouse aortic ring assay: a new approach of the molecular genetics of angiogenesis. Biol Proced Online 4:24鈥?1 CrossRef
    40. Akhtar N, Dickerson EB, Auerbach R (2002) The sponge/matrigel angiogenesis assay. Angiogenesis 5:75鈥?0 CrossRef
    41. Bain G, Ray WJ, Yao M, Gottlieb DI (1994) From embryonal carcinoma cells to neurons: the P19 pathway. BioEssays 16:343鈥?48 CrossRef
    42. McBurney MW, Rogers BJ (1982) Isolation of male embryonal carcinoma cells and their chromosome replication patterns. Dev Biol 89:503鈥?08 CrossRef
    43. Reynolds BA, Weiss S (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707鈥?710 CrossRef
    44. Kurosawa H (2007) Methods for inducing embryoid body formation: in vitro differentiation system of embryonic stem cells. J Biosci Bioeng 103:389鈥?98 CrossRef
    45. Brewer GJ, Torricelli JR, Evege EK, Price PJ (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 35:567鈥?76 CrossRef
    46. Cho GW, Kang BY, Kim SH (2010) Human angiogenin presents neuroprotective and migration effects in neuroblastoma cells. Mol Cell Biochem 340:133鈥?41 CrossRef
    47. Li S, Yu W, Kishikawa H, Hu GF (2010) Angiogenin prevents serum withdrawal-induced apoptosis of P19 embryonal carcinoma cells. FEBS J 277:3575鈥?587 CrossRef
    48. Sebastia J, Kieran D, Breen B, King MA, Netteland DF, Joyce D, Fitzpatrick SF, Taylor CT, Prehn JH (2009) Angiogenin protects motoneurons against hypoxic injury. Cell Death Differ 16:1238鈥?247 CrossRef
    49. Steidinger TU, Standaert DG, Yacoubian TA (2011) A neuroprotective role for angiogenin in models of Parkinson鈥檚 disease. J Neurochem 116:334鈥?41 CrossRef
    50. Subramanian V, Crabtree B, Acharya KR (2008) Human angiogenin is a neuroprotective factor and amyotrophic lateral sclerosis associated angiogenin variants affect neurite extension/pathfinding and survival of motor neurons. Hum Mol Genet 17:130鈥?49 CrossRef
    51. Moroianu J, Riordan JF (1994) Nuclear translocation of angiogenin in proliferating endothelial cells is essential to its angiogenic activity. Proc Natl Acad Sci USA 91:1677鈥?681 CrossRef
    52. Tsuji T, Sun Y, Kishimoto K, Olson KA, Liu S, Hirukawa S, Hu GF (2005) Angiogenin is translocated to the nucleus of HeLa cells and is involved in ribosomal RNA transcription and cell proliferation. Cancer Res 65:1352鈥?360 CrossRef
    53. Tu PH, Raju P, Robinson KA, Gurney ME, Trojanowski JQ, Lee VM (1996) Transgenic mice carrying a human mutant superoxide dismutase transgene develop neuronal cytoskeletal pathology resembling human amyotrophic lateral sclerosis lesions. Proc Natl Acad Sci USA 93:3155鈥?160 CrossRef
    54. Gurney ME, Cutting FB, Zhai P, Doble A, Taylor CP, Andrus PK, Hall ED (1996) Benefit of vitamin E, riluzole, and gabapentin in a transgenic model of familial amyotrophic lateral sclerosis. Ann Neurol 39:147鈥?57 CrossRef
    55. Danzeisen R, Schwalenstoecker B, Gillardon F, Buerger E, Krzykalla V, Klinder K, Schild L, Hengerer B, Ludolph AC, Dorner-Ciossek C et al (2006) Targeted antioxidative and neuroprotective properties of the dopamine agonist pramipexole and its nondopaminergic enantiomer SND919CL2x [(+)2-amino-4,5,6,7-tetrahydro-6-Lpropylamino-benzathiazole dihydrochloride]. J Pharmacol Exp Ther 316:189鈥?99 CrossRef
    56. Carmeliet P (2008) Neuro-vascular link: from genetic insights to therapeutic perspectives. Bull Mem Acad R Med Belg 163:445鈥?51 (discussion 451鈥?42)
    57. Segura I, De Smet F, Hohensinner PJ, Ruiz de Almodovar C, Carmeliet P (2009) The neurovascular link in health and disease: an update. Trends Mol Med 15:439鈥?51 CrossRef
    58. Tran TS, Kolodkin AL, Bharadwaj R (2007) Semaphorin regulation of cellular morphology. Annu Rev Cell Dev Biol 23:263鈥?92 CrossRef
    59. Lambrechts D, Lafuste P, Carmeliet P, Conway EM (2006) Another angiogenic gene linked to amyotrophic lateral sclerosis. Trends Mol Med 12:345鈥?47 CrossRef
    60. Oosthuyse B, Moons L, Storkebaum E, Beck H, Nuyens D, Brusselmans K, Van Dorpe J, Hellings P, Gorselink M, Heymans S et al (2001) Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration. Nat Genet 28:131鈥?38 CrossRef
    61. Zheng C, Nennesmo I, Fadeel B, Henter JI (2004) Vascular endothelial growth factor prolongs survival in a transgenic mouse model of ALS. Ann Neurol 56:564鈥?67 CrossRef
    62. Shapiro R, Vallee BL (1989) Site-directed mutagenesis of histidine-13 and histidine-114 of human angiogenin. Alanine derivatives inhibit angiogenin-induced angiogenesis. Biochemistry 28:7401鈥?408 CrossRef
    63. Hu GF, Riordan JF, Vallee BL (1997) A putative angiogenin receptor in angiogenin-responsive human endothelial cells. Proc Natl Acad Sci USA 94:2204鈥?209 CrossRef
    64. Bratt-Leal AM, Carpenedo RL, McDevitt TC (2009) Engineering the embryoid body microenvironment to direct embryonic stem cell differentiation. Biotechnol Prog 25:43鈥?1 CrossRef
    65. Kawasaki H, Mizuseki K, Nishikawa S, Kaneko S, Kuwana Y, Nakanishi S, Nishikawa SI, Sasai Y (2000) Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28:31鈥?0 CrossRef
    66. Li S, Yu W, Hu GF (2011) Angiogenin inhibits nuclear translocation of apoptosis inducing factor in a Bcl-2-dependent manner. J Cell Physiol 227(4):1639鈥?644 CrossRef
    67. Greenway MJ, Alexander MD, Ennis S, Traynor BJ, Corr B, Frost E, Green A, Hardiman O (2004) A novel candidate region for ALS on chromosome 14q11.2. Neurology 63:1936鈥?938 CrossRef
  • 作者单位:Shuping Li (1) (2)
    Jinghao Sheng (1) (3)
    Jamie K. Hu (1)
    Wenhao Yu (1)
    Hiroko Kishikawa (1)
    Miaofen G. Hu (1)
    Kaori Shima (4)
    David Wu (5)
    Zhengping Xu (3)
    Winnie Xin (6)
    Katherine B. Sims (6)
    John E. Landers (7)
    Robert H. Brown Jr. (7)
    Guo-fu Hu (1)

    1. Molecular Oncology Research Institute, Tufts Medical Center, 800 Washington Street, Box 5069, Boston, MA, 02111, USA
    2. State Key Laboratory for Diagnosis and Treatment of Infectious Disease, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China
    3. Institute of Environmental Medicine, Zhejiang University School of Medicine, Hangzhou, China
    4. Division of Oral Pathology, Kagoshima University Graduate School of Medical and Dental Sciences, Kagoshima, Japan
    5. Department of Laboratory Medicine, University of Washington, Seattle, WA, USA
    6. Department of Neurology, Center for Human Genetic Research, Massachusetts General Hospital, Boston, MA, USA
    7. Department of Neurology, University of Massachusetts Medical School, Worcester, MA, USA
  • ISSN:1573-7209
文摘
Altered RNA processing is an underlying mechanism of amyotrophic lateral sclerosis (ALS). Missense mutations in a number of genes involved in RNA function and metabolisms are associated with ALS. Among these genes is angiogenin (ANG), the fifth member of the vertebrate-specific, secreted ribonuclease superfamily. ANG is an angiogenic ribonuclease, and both its angiogenic and ribonucleolytic activities are important for motor neuron health. Ribonuclease 4 (RNASE4), the fourth member of this superfamily, shares the same promoters with ANG and is co-expressed with ANG. However, the biological role of RNASE4 is unknown. To determine whether RNASE4 is involved in ALS pathogenesis, we sequenced the coding region of RNASE4 in ALS and control subjects and characterized the angiogenic, neurogenic, and neuroprotective activities of RNASE4 protein. We identified an allelic association of SNP rs3748338 with ALS and demonstrated that RNASE4 protein is able to induce angiogenesis in in vitro, ex vivo, and in vivo assays. RNASE4 also induces neural differentiation of P19 mouse embryonal carcinoma cells and mouse embryonic stem cells. Moreover, RNASE4 not only stimulates the formation of neurofilaments from mouse embryonic cortical neurons, but also protects hypothermia-induced degeneration. Importantly, systemic treatment with RNASE4 protein slowed weight loss and enhanced neuromuscular function of SOD1 G93A mice.
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