Neurons derived from patients with bipolar disorder divide into intrinsically different sub-populations of neurons, predicting the patients' responsiveness to lithium

Molecular Psychiatry

Volumn 23, Issue 6, 2018, Pages 1453-1465

  Stern, S ^a   Santos, R ^a,b   Marchetto, M C ^a   Mendes, A P D ^a   Rouleau, G A ^c   Biesmans, S ^d   Wang, Q W ^e   Yao, J ^e   Charnay, P ^b   Bang, A G ^d   Alda, M ^f   Gage, F H ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b ECOLE NORMALE SUPÉRIEURE   (France)

^c MCGILL UNIVERSITY   (Canada)

^d BURNHAM INSTITUTE   (United States)

^e TSINGHUA UNIVERSITY   (China)

^f DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

LITHIUM DERIVATIVE; LITHIUM; NEUROLEPTIC AGENT; PHARMACOLOGICAL BIOMARKER; TRANQUILIZER;

AFTERHYPERPOLARIZATION; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; BAYESIAN LEARNING; BIPOLAR DISORDER; CELL SUBPOPULATION; CLINICAL ARTICLE; CLINICAL FEATURE; COHORT ANALYSIS; CONTROLLED STUDY; DENTATE GYRUS; ELECTROPHYSIOLOGY; EVOKED RESPONSE; FIBROBLAST; HUMAN; INDUCED PLURIPOTENT STEM CELL; NERVE CELL; NERVE EXCITABILITY; PRIORITY JOURNAL; TREATMENT RESPONSE; WHOLE CELL PATCH CLAMP; ADULT; CASE CONTROL STUDY; CELL DIFFERENTIATION; DRUG EFFECT; FEMALE; GENETICS; HIPPOCAMPUS; MALE; METABOLISM; PATCH CLAMP TECHNIQUE; PHYSIOLOGY;

ADULT; ANTIMANIC AGENTS; ANTIPSYCHOTIC AGENTS; BIOMARKERS, PHARMACOLOGICAL; BIPOLAR DISORDER; CASE-CONTROL STUDIES; CELL DIFFERENTIATION; DENTATE GYRUS; FEMALE; HIPPOCAMPUS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; LITHIUM; LITHIUM COMPOUNDS; MALE; NEURONS; PATCH-CLAMP TECHNIQUES;

EID: 85014026997     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2016.260     Document Type: Article

References (61)

1. Angst J. The emerging epidemiology of hypomania and bipolar II disorder. J Affect Disord 1998; 50: 143-151.
2. Hirschfeld RM, Calabrese JR, Weissman MM, Reed M, Davies MA, Frye MA et al. Screening for bipolar disorder in the community. J Clin Psychiatry 2003; 64: 53-59.
3. Merikangas KR, Akiskal HS, Angst J, Greenberg PE, Hirschfeld RM, Petukhova M et al. Lifetime and 12-month prevalence of bipolar spectrum disorder in the National Comorbidity Survey replication. Arch Gen Psychiatry 2007; 64: 543-552.
4. Belmaker RH. Bipolar disorder. N Engl J Med 2004; 351: 476-486.
5. Judd LL, Akiskal HS, Schettler PJ, Endicott J, Maser J, Solomon DA et al. The long-term natural history of the weekly symptomatic status of bipolar I disorder. Arch Gen Psychiatry 2002; 59: 530-537.
6. Vandeleur CL, Merikangas KR, Strippoli MP, Castelao E, Preisig M. Specificity of psychosis, mania and major depression in a contemporary family study. Mol Psychiatry 2014; 19: 209-213.
7. Baethge C, Baldessarini RJ, Freudenthal K, Streeruwitz A, Bauer M, Bschor T. Hallucinations in bipolar disorder: characteristics and comparison to unipolar depression and schizophrenia. Bipolar Disord 2005; 7: 136-145.
8. Harris EC, Barraclough B. Suicide as an outcome for mental disorders. A meta-analysis. Br J Psychiatry 1997; 170: 205-228.
9. Tondo L, Isacsson G, Baldessarini R. Suicidal behaviour in bipolar disorder: risk and prevention. CNS Drugs 2003; 17: 491-511.
10. Geddes JR, Burgess S, Hawton K, Jamison K, Goodwin GM. Long-term lithium therapy for bipolar disorder: systematic review and meta-analysis of randomized controlled trials. Am J Psychiatry 2004; 161: 217-222.
11. Burgess S, Geddes J, Hawton K, Townsend E, Jamison K, Goodwin G. Lithium for maintenance treatment of mood disorders. Cochrane Database Syst Rev 2001; (3): CD003013.
12. Klein PS, Melton DA. A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci USA 1996; 93: 8455-8459.
13. Jope RS. Anti-bipolar therapy: mechanism of action of lithium. Mol Psychiatry 1999; 4: 117-128.
14. Chiu CT, Wang Z, Hunsberger JG, Chuang DM. Therapeutic potential of mood stabilizers lithium and valproic acid: beyond bipolar disorder. Pharmacol Rev 2013; 65: 105-142.
15. Machado-Vieira R, Manji HK, Zarate CA Jr. The role of lithium in the treatment of bipolar disorder: convergent evidence for neurotrophic effects as a unifying hypothesis. Bipolar Disord 2009; 11 (Suppl. 2): 92-109.
16. Breen MS, White CH, Shekhtman T, Lin K, Looney D, Woelk CH et al. Lithiumresponsive genes and gene networks in bipolar disorder patient-derived lymphoblastoid cell lines. Pharmacogenom J 2016; 16: 446-453.
17. Viguera AC, Tondo L, Baldessarini RJ. Sex differences in response to lithium treatment. Am J Psychiatry 2000; 157: 1509-1511.
18. Tohen M, Greil W, Calabrese JR, Sachs GS, Yatham LN, Oerlinghausen BM et al. Olanzapine versus lithium in the maintenance treatment of bipolar disorder: a 12-month, randomized, double-blind, controlled clinical trial. Am J Psychiatry 2005; 162: 1281-1290.
19. Smoller JW, Finn CT. Family, twin, and adoption studies of bipolar disorder. Am J Med Genet C 2003; 123C: 48-58.
20. McGuffin P, Rijsdijk F, Andrew M, Sham P, Katz R, Cardno A. The heritability of bipolar affective disorder and the genetic relationship to unipolar depression. Arch Gen Psychiatry 2003; 60: 497-502.
21. Kieseppa T, Partonen T, Haukka J, Kaprio J, Lonnqvist J. High concordance of bipolar I disorder in a nationwide sample of twins. Am J Psychiatry 2004; 161: 1814-1821.
22. International Schizophrenia C, Purcell SM, Wray NR, Stone JL, Visscher PM, O'Donovan MC et al. Common polygenic variation contributes to risk of schizophrenia and bipolar disorder. Nature 2009; 460: 748-752.
23. Craddock N, Sklar P. Genetics of bipolar disorder. Lancet 2013; 381: 1654-1662.
24. Psychiatric GCBDWG. Large-scale genome-wide association analysis of bipolar disorder identifies a new susceptibility locus near ODZ4. Nat Genet 2011; 43: 977-983.
25. Ferreira MA, O'Donovan MC, Meng YA, Jones IR, Ruderfer DM, Jones L et al. Collaborative genome-wide association analysis supports a role for ANK3 and CACNA1C in bipolar disorder. Nat Genet 2008; 40: 1056-1058.
26. Carter CJ. Multiple genes and factors associated with bipolar disorder converge on growth factor and stress activated kinase pathways controlling translation initiation: implications for oligodendrocyte viability. Neurochem Int 2007; 50: 461-490.
27. Ogden CA, Rich ME, Schork NJ, Paulus MP, Geyer MA, Lohr JB et al. Candidate genes, pathways and mechanisms for bipolar (manic-depressive) and related disorders: an expanded convergent functional genomics approach. Mol Psychiatry 2004; 9: 1007-1029.
28. Nestler EJ, Hyman SE. Animal models of neuropsychiatric disorders. Nat Neurosci 2010; 13: 1161-1169.
29. Einat H, Manji HK. Cellular plasticity cascades: genes-to-behavior pathways in animal models of bipolar disorder. Biol Psychiatry 2006; 59: 1160-1171.
30. Rajkowska G, Halaris A, Selemon LD. Reductions in neuronal and glial density characterize the dorsolateral prefrontal cortex in bipolar disorder. Biol Psychiatry 2001; 49: 741-752.
31. Bertolino A, Frye M, Callicott JH, Mattay VS, Rakow R, Shelton-Repella J et al. Neuronal pathology in the hippocampal area of patients with bipolar disorder: a study with proton magnetic resonance spectroscopic imaging. Biol Psychiatry 2003; 53: 906-913.
32. Bouras C, Kovari E, Hof PR, Riederer BM, Giannakopoulos P. Anterior cingulate cortex pathology in schizophrenia and bipolar disorder. Acta Neuropathol 2001; 102: 373-379.
33. Rajkowska G. Postmortem studies in mood disorders indicate altered numbers of neurons and glial cells. Biol Psychiatry 2000; 48: 766-777.
34. Cotter D, Mackay D, Landau S, Kerwin R, Everall I. Reduced glial cell density and neuronal size in the anterior cingulate cortex in major depressive disorder. Arch Gen Psychiatry 2001; 58: 545-553.
35. Askland K, Read C, Moore J. Pathways-based analyses of whole-genome association study data in bipolar disorder reveal genes mediating ion channel activity and synaptic neurotransmission. Hum Genet 2009; 125: 63-79.
36. Mahmood T, Silverstone T. Serotonin and bipolar disorder. J Affect Disord 2001; 66: 1-11.
37. Scarr E, Pavey G, Sundram S, MacKinnon A, Dean B. Decreased hippocampal NMDA, but not kainate or AMPA receptors in bipolar disorder. Bipolar Disord 2003; 5: 257-264.
38. Benes FM, Berretta S. GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacology 2001; 25: 1-27.
39. Guidotti A, Auta J, Davis JM, Di-Giorgi-Gerevini V, Dwivedi Y, Grayson DR et al. Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch Gen Psychiatry 2000; 57: 1061-1069.
40. Fattal O, Link J, Quinn K, Cohen BH, Franco K. Psychiatric comorbidity in 36 adults with mitochondrial cytopathies. CNS Spectrums 2007; 12: 429-438.
41. Marazziti D, Baroni S, Picchetti M, Landi P, Silvestri S, Vatteroni E et al. Psychiatric disorders and mitochondrial dysfunctions. Eur Rev Med Pharmacol Sci 2012; 16: 270-275.
42. Mertens J, Wang QW, Kim Y, Yu DX, Pham S, Yang B et al. Differential responses to lithium in hyperexcitable neurons from patients with bipolar disorder. Nature 2015; 527: 95-99.
43. Harrison PJ, Cader MZ, Geddes JR. Reprogramming psychiatry: stem cells and bipolar disorder. Lancet 2016; 387: 823-825.
44. Choi SM, Liu H, Chaudhari P, Kim Y, Cheng L, Feng J et al. Reprogramming of EBV-immortalized B-lymphocyte cell lines into induced pluripotent stem cells. Blood 2011; 118: 1801-1805.
45. Rajesh D, Dickerson SJ, Yu J, Brown ME, Thomson JA, Seay NJ. Human lymphoblastoid B-cell lines reprogrammed to EBV-free induced pluripotent stem cells. Blood 2011; 118: 1797-1800.
46. Mamdani F, Alda M, Grof P, Young LT, Rouleau G, Turecki G. Lithium response and genetic variation in the CREB family of genes. Am J Med Genet B 2008; 147B: 500-504.
47. Spitzer RL, Endicott J, Robins E. Research diagnostic criteria: rationale and reliability. Arch Gen Psychiatry 1978; 35: 773-782.
48. Endicott J, Spitzer RL. A diagnostic interview: the schedule for affective disorders and schizophrenia. Arch Gen Psychiatry 1978; 35: 837-844.
49. Lopez de Lara C, Jaitovich-Groisman I, Cruceanu C, Mamdani F, Lebel V, Yerko V et al. Implication of synapse-related genes in bipolar disorder by linkage and gene expression analyses. Int J Neuropsychopharmacol 2010; 13: 1397-1410.
50. Manchia M, Adli M, Akula N, Ardau R, Aubry JM, Backlund L et al. Assessment of response to lithium maintenance treatment in bipolar disorder: a Consortium On Lithium Genetics (ConLiGen) Report. PLoS One 2013; 8: e65636.
51. Garnham J, Munro A, Slaney C, Macdougall M, Passmore M, Duffy A et al. Prophylactic treatment response in bipolar disorder: results of a naturalistic observation study. J affect Disord 2007; 104: 185-190.
52. Grof P, Cavazzoni P, Grof E, Garnham J, MacDougall M, O'Donovan C, Alda M. Is response to prophylactic lithium a familial trait? J Clin Psychiatry 2002; 63: 942-947.
53. Okita K, Matsumura Y, Sato Y, Okada A, Morizane A, Okamoto S et al. A more efficient method to generate integration-free human iPS cells. Nat Methods 2011; 8: 409-412.
54. Rudy B. Diversity and ubiquity of K channels. Neuroscience 1988; 25: 729-749.
55. Yu DX, Di Giorgio FP, Yao J, Marchetto MC, Brennand K, Wright R et al. Modeling hippocampal neurogenesis using human pluripotent stem cells. Stem Cell Rep 2014; 2: 295-310.
56. Stern S, Segal M, Moses E. Involvement of potassium and cation channels in hippocampal abnormalities of embryonic Ts65Dn and Tc1 trisomic mice. EBioMedicine 2015; 2: 1048-1062.
57. Jan LY, Jan YN. Voltage-gated and inwardly rectifying potassium channels. J Physiol 1997; 505(Part 2): 267-282.
58. Erisir A, Lau D, Rudy B, Leonard CS. Function of specific K(+) channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J Neurophysiol 1999; 82: 2476-2489.
59. Connors BW, Gutnick MJ. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 1990; 13: 99-104.
60. Martina M, Schultz JH, Ehmke H, Monyer H, Jonas P. Functional and molecular differences between voltage-gated K+ channels of fast-spiking interneurons and pyramidal neurons of rat hippocampus. J Neurosci 1998; 18: 8111-8125.
61. Rudy B, Chow A, Lau D, Amarillo Y, Ozaita A, Saganich M et al. Contributions of Kv3 channels to neuronal excitability. Ann NY Acad Sci 1999; 868: 304-343.