Alzheimer-related protein APL-1 modulates lifespan through heterochronic gene regulation in Caenorhabditis elegans

Aging Cell

Volumn 15, Issue 6, 2016, Pages 1051-1062

  Ewald, Collin Y ^a,b,c   Marfil, Vanessa ^b   Li, Chris ^a,b  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b CITY COLLEGE OF NEW YORK   (United States)

^c ETH ZURICH   (Switzerland)

Author keywords

Alzheimer's disease; APL 1; APP; FOXO transcription factor DAF 16; heat shock factor HSF 1; heterochronic gene LIN 14; lifespan; vitamin D like nuclear hormone receptor DAF 12

Indexed keywords

ALZHEIMER RELATED PROTEIN 1; AMYLOID PRECURSOR PROTEIN; HETEROCHRONIC TRANSCRIPTION FACTOR LIN 14; PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG; VITAMIN D;

ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DOWN REGULATION; ECTOPIC EXPRESSION; ENDOPLASMIC RETICULUM; GENE CONTROL; GENE OVEREXPRESSION; LIFE EXTENSION; LIFESPAN; LONGEVITY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SUBCUTANEOUS TISSUE; UNFOLDED PROTEIN RESPONSE;

EID: 84983287971     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12509     Document Type: Article

References (45)

1. Alzheimer's Association (2015) 2015 Alzheimer's disease facts and figures. Alzheimers Dement. 11, 332–384.
2. Ambros V, Horvitz HR (1984) Heterochronic mutants of the nematode Caenorhabditis elegans. Science 226, 409–416.
3. Ambros V, Horvitz HR (1987) The lin-14 locus of Caenorhabditis elegans controls the time of expression of specific postembryonic developmental events. Genes Dev. 1, 398–414.
4. Antebi A (2013) Regulation of longevity by the reproductive system. Exp. Gerontol. 48, 596–602.
5. Boehm M, Slack F (2005) A developmental timing microRNA and its target regulate life span in C. elegans. Science 310, 1954–1957.
6. Cabrejo L, Guyant-Maréchal L, Laquerrière A, Vercelletto M, De la Fournière F, Thomas-Antérion C, Verny C, Letournel F, Pasquier F, Vital A, Checler F, Frebourg T, Campion D, Hannequin D (2006) Phenotype associated with APP duplication in five families. Brain 129, 2966–2976.
7. Daigle I, Li C (1993) apl-1, a Caenorhabditis elegans gene encoding a protein related to the human beta-amyloid protein precursor. Proc. Natl Acad. Sci. USA 90, 12045–12049.
8. Ewald CY, Li C (2010) Understanding the molecular basis of Alzheimer's disease using a Caenorhabditis elegans model system. Brain Struct. Funct. 214, 263–283.
9. Ewald CY, Li C (2012) Caenorhabditis elegans as a model organism to study APP function. Exp. Brain Res. 217, 397–411.
10. Ewald CY, Cheng R, Tolen L, Shah V, Gillani A, Nasrin A, Li C (2012a) Pan-neuronal expression of APL-1, an APP-related protein, disrupts olfactory, gustatory, and touch plasticity in Caenorhabditis elegans. J. Neurosci. 32, 10156–10169.
11. Ewald CY, Raps DA, Li C (2012b) APL-1, the Alzheimer's Amyloid precursor protein in Caenorhabditis elegans, modulates multiple metabolic pathways throughout development. Genetics 191, 493–507.
12. Ewald CY, Landis JN, Porter Abate J, Murphy CT, Blackwell TK (2015) Dauer-independent insulin/IGF-1-signalling implicates collagen remodelling in longevity. Nature 519, 97–101.
13. Gems D, Riddle DL (2000) Defining wild-type life span in Caenorhabditis elegans. J. Gerontol. A Biol. Sci. Med. Sci. 55, B215–B219.
14. Heestand BN, Shen Y, Liu W, Magner DB, Storm N, Meharg C, Habermann B, Antebi A (2013) Dietary restriction induced longevity is mediated by nuclear receptor NHR-62 in Caenorhabditis elegans. S. K. Kim, ed. PLoS Genet. 9, e1003651.
15. Herms J, Gajic V, Hainfellner J, Aguzzi A, Rülicke T, von Kretzschmar H, von Koch C, Sisodia S, Tremml P, Lipp HP, Wolfer DP (2000) Mice with combined gene knock-outs reveal essential and partially redundant functions of amyloid precursor protein family members. J. Neurosci. 20, 7951–7963.
16. Herms J, Anliker B, Heber S, Ring S, Fuhrmann M, Kretzschmar H, Sisodia S, Müller U (2004) Cortical dysplasia resembling human type 2 lissencephaly in mice lacking all three APP family members. EMBO J. 23, 4106–4115.
17. Hong Y, Lee RC, Ambros V (2000) Structure and function analysis of LIN-14, a temporal regulator of postembryonic developmental events in Caenorhabditis elegans. Mol. Cell. Biol. 20, 2285–2295.
18. Hoogewijs D, Houthoofd K, Matthijssens F, Vandesompele J, Vanfleteren JR (2008) Selection and validation of a set of reliable reference genes for quantitative sod gene expression analysis in C. elegans. BMC Mol. Biol. 9, 9.
19. Hoopes JT, Liu X, Xu X, Demeler B, Folta-Stogniew E, Li C, Ha Y (2010) Structural characterization of the E2 domain of APL-1, a Caenorhabditis elegans homolog of human amyloid precursor protein, and its heparin binding site. J. Biol. Chem. 285, 2165–2173.
20. Hornsten A, Lieberthal J, Fadia S, Malins R, Ha L, Xu X, Daigle I, Markowitz M, O'Connor G, Plasterk R, Li C (2007) APL-1, a Caenorhabditis elegans protein related to the human beta-amyloid precursor protein, is essential for viability. Proc. Natl Acad. Sci. USA 104, 1971–1976.
21. Hristova M, Birse D, Hong Y, Ambros V (2005) The Caenorhabditis elegans heterochronic regulator LIN-14 is a novel transcription factor that controls the developmental timing of transcription from the insulin/insulin-like growth factor gene ins-33 by direct DNA binding. Mol. Cell. Biol. 25, 11059–11072.
22. Hsiao KK, Borchelt DR, Olson K, Johannsdottir R, Kitt C, Yunis W, Xu S, Eckman C, Younkin S, Price D (1995) Age-related CNS disorder and early death in transgenic FVB/N mice overexpressing Alzheimer amyloid precursor proteins. Neuron 15, 1203–1218.
23. Ibáñez-Ventoso C, Driscoll M (2009) MicroRNAs in C. elegans aging: molecular insurance for robustness? Curr. Genomics 10, 144–153.
24. Ibáñez-Ventoso C, Yang M, Guo S, Robins H, Padgett RW, Driscoll M (2006) Modulated microRNA expression during adult lifespan in Caenorhabditis elegans. Aging Cell 5, 235–246.
25. Keightley PD, Caballero A (1997) Genomic mutation rates for lifetime reproductive output and lifespan in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 94, 3823–3827.
26. Kenyon CJ (2010) The genetics of ageing. Nature 464, 504–512.
27. Kirkwood TB, Holliday R (1979) The evolution of ageing and longevity. Proc. R. Soc. Lond. B Biol. Sci. 205, 531–546.
28. von Koch CS, Zheng H, Chen H, Trumbauer M, Thinakaran G, Van Der Ploeg LH, Price DL, Sisodia SS (1997) Generation of APLP2 KO mice and early postnatal lethality in APLP2/APP double KO mice. Neurobiol. Aging 18, 661–669.
29. Korbel JO, Tirosh-Wagner T, Urban AE, Chen X-N, Kasowski M, Dai L, Grubert F, Erdman C, Gao MC, Lange K, Sobel EM, Barlow GM, Aylsworth AS, Carpenter NJ, Clark RD, Cohen MY, Doran E, Falik-Zaccai T, Lewin SO, Lott IT, McGillivray BC, Moeschler JB, Pettenati MJ, Pueschel SM, Rao KW, Shaffer LG, Shohat M, Van Riper AJ, Warburton D, Weissman S, Gerstein MB, Snyder M, Korenberg JR (2009) The genetic architecture of Down syndrome phenotypes revealed by high-resolution analysis of human segmental trisomies. Proc. Natl Acad. Sci. USA 106, 12031–12036.
30. Labbadia J, Morimoto RI (2014) Proteostasis and longevity: when does aging really begin? F1000Prime Rep. 6, 7.
31. Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843–854.
32. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, Li H, Kenyon CJ (2003) Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424, 277–283.
33. Niwa R, Zhou F, Li C, Slack FJ (2008) The expression of the Alzheimer's amyloid precursor protein-like gene is regulated by developmental timing microRNAs and their targets in Caenorhabditis elegans. Dev. Biol. 315, 418–425.
34. Olsson-Carter K, Slack FJ (2010) A developmental timing switch promotes axon outgrowth independent of known guidance receptors. K. Olsson-Carter & F. J. Slack, eds. PLoS Genet. 6, e1001054.
35. Rougvie AE, Moss EG (2013) Developmental transitions in C. elegans larval stages. Curr. Top. Dev. Biol. 105, 153–180.
36. Rovelet-Lecrux A, Hannequin D, Raux G, Le Meur N, Laquerrière A, Vital A, Dumanchin C, Feuillette S, Brice A, Vercelletto M, Dubas F, Frebourg T, Campion D (2006) APP locus duplication causes autosomal dominant early-onset Alzheimer disease with cerebral amyloid angiopathy. Nat. Genet. 38, 24–26.
37. Selkoe DJ, Hardy J (2016) The amyloid hypothesis of Alzheimer's disease at 25 years. EMBO Mol. Med. 8, 595–608.
38. Shariati SAM, De Strooper B (2013) Redundancy and divergence in the amyloid precursor family. FEBS Letters 587, 2036–2045.
39. Shen Y, Wollam J, Magner D, Karalay O, Antebi A (2012) A steroid receptor-microRNA switch regulates life span in response to signals from the gonad. Science 338, 1472–1476.
40. Sleegers K, Brouwers N, Gijselinck I, Theuns J, Goossens D, Wauters J, Del-Favero J, Cruts M, van Duijn CM, Van Broeckhoven C (2006) APP duplication is sufficient to cause early onset Alzheimer's dementia with cerebral amyloid angiopathy. Brain 129, 2977–2983.
41. Tanzi RE (2012) The genetics of Alzheimer disease. Cold Spring Harb. Perspect Med. 2, a006296.
42. Tanzi RE, Gusella JF, Watkins PC, Bruns GA, St George Hyslop P, Van Keuren ML, Patterson D, Pagan S, Kurnit DM, Neve RL (1987) Amyloid beta protein gene: cDNA, mRNA distribution, and genetic linkage near the Alzheimer locus. Science 235, 880–884.
43. Taylor RC, Dillin A (2013) XBP-1 is a cell-nonautonomous regulator of stress resistance and longevity. Cell 153, 1435–1447.
44. Weyer SW, Klevanski M, Delekate A, Voikar V, Aydin D, Hick M, Filippov M, Drost N, Schaller KL, Saar M, Vogt MA, Gass P, Samanta A, schke AJA, Korte M, Wolfer DP, Caldwell JH, Müller UC (2011) APP and APLP2 are essential at PNS and CNS synapses for transmission, spatial learning and LTP. EMBO J. 30, 2266–2280.
45. Wiese M, Antebi A, Zheng H (2010) Intracellular trafficking and synaptic function of APL-1 in Caenorhabditis elegans. C.-X. Gong, ed. PLoS One 5, e12790.