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2. No Reliable Association between Runs of Homozygosity and Schizophrenia in a Well-Powered Replication Study

Author

Johnson, Emma C., Bjelland, Douglas W., Howrigan, Daniel P., Abdellaoui, Abdel, Breen, Gerome, Borglum, Anders, Cichon, Sven, Degenhardt, Franziska, Forstner, Andreas J., Frank, Josef, Genovese, Giulio, Heilmann-Heimbach, Stefanie, Herms, Stefan, Hoffman, Per, Maier, Wolfgang, Mattheisen, Manuel, Morris, Derek, Mowry, Bryan, Müller-Mhysok, Betram, Neale, Benjamin, Nenadic, Igor, Nöthen, Markus M., O’Dushlaine, Colm, Rietschel, Marcella, Ruderfer, Douglas M., Rujescu, Dan, Schulze, Thomas G., Simonson, Matthew A., Stahl, Eli, Strohmaier, Jana, Witt, Stephanie H., Ripke, Stephan, Neale, Benjamin M., Corvin, Aiden, Walters, James T R, Farh, Kai How, Holmans, Peter A., Lee, Phil, Bulik-Sullivan, Brendan, Collier, David A., Huang, Hailiang, Pers, Tune H., Agartz, Ingrid, Agerbo, Esben, Albus, Margot, Alexander, Madeline, Amin, Farooq, Bacanu, Silviu A., Begemann, Martin, Belliveau, Richard A., Bene, Judit, Bergen, Sarah E., Bevilacqua, Elizabeth, Bigdeli, Tim B., Black, Donald W., Bruggeman, Richard, Buccola, Nancy G., Buckner, Randy L., Byerley, William, Cahn, Wiepke, Cai, Guiqing, Campion, Dominique, Cantor, Rita M., Carr, Vaughan J., Carrera, Noa, Catts, Stanley V., Chambert, Kimberly D., Chan, Raymond C K, Chen, Ronald Y L, Chen, Eric Y H, Cheng, Wei, Cheung, Eric F C, Chong, Siow Ann, Robert Cloninger, C., Cohen, David, Cohen, Nadine, Cormican, Paul, Craddock, Nick, Crowley, James J., Curtis, David, Davidson, Michael, Davis, Kenneth L., Del Favero, Jurgen, Demontis, Ditte, Dikeos, Dimitris, Dinan, Timothy, Djurovic, Srdjan, Donohoe, Gary, Drapeau, Elodie, Duan, Jubao, Dudbridge, Frank, Durmishi, Naser, Eichhammer, Peter, Eriksson, Johan, Escott-Price, Valentina, Essioux, Laurent, Fanous, Ayman H., Farrell, Martilias S., Franke, Lude, Freedman, Robert, Freimer, Nelson B., Friedl, Marion, Friedman, Joseph I., Fromer, Menachem, Georgieva, Lyudmila, Giegling, Ina, Giusti-Rodríguez, Paola, Godard, Stephanie, Goldstein, Jacqueline I., Golimbet, Vera, Gopal, Srihari, Gratten, Jacob, de Haan, Lieuwe, Hammer, Christian, Hamshere, Marian L., Hansen, Mark, Hansen, Thomas, Haroutunian, Vahram, Hartmann, Annette M., Henskens, Frans A., Hirschhorn, Joel N., Hoffmann, Per, Hofman, Andrea, Hollegaard, Mads V., Hougaard, David M., Ikeda, Masashi, Joa, Inge, Julià, Antonio, Kahn, René S., Kalaydjieva, Luba, Karachanak-Yankova, Sena, Karjalainen, Juha, Kavanagh, David, Kennedy, James L., Khrunin, Andrey, Kim, Yunjung, Klovins, Janis, Knowles, James A., Konte, Bettina, Kucinskas, Vaidutis, Kucinskiene, Zita Ausrele, Kuzelova-Ptackova, Hana, Kähler, Anna K., Laurent, Claudine, Chee Keong, Jimmy Lee, Hong Lee, S., Legge, Sophie E., Lerer, Bernard, Li, Miaoxin, Li, Tao, Liang, Kung Yee, Lieberman, Jeffrey, Limborska, Svetlana, Loughland, Carmel M., Lubinski, Jan, Lönnqvist, Jouko, Macek, Milan, Magnusson, Patrik K E, Maher, Brion S., Mallet, Jacques, Marsal, Sara, Mattingsdal, Morten, McCarley, Robert W., McDonald, Colm, McIntosh, Andrew M., Meier, Sandra, Meijer, Carin J., Melegh, Bela, Melle, Ingrid, Mesholam-Gately, Raquelle I., Metspalu, Andres, Michie, Patricia T., Milani, Lili, Milanova, Vihra, Mokrab, Younes, Morris, Derek W., Mors, Ole, Murphy, Kieran C., Murray, Robin M., Myin-Germeys, Inez, Müller-Myhsok, Bertram, Nelis, Mari, Nertney, Deborah A., Nestadt, Gerald, Nicodemus, Kristin K., Nikitina-Zake, Liene, Nisenbaum, Laura, Nordin, Annelie, O'Callaghan, Eadbhard, O'Dushlaine, Colm, Anthony O'Neill, F., Oh, Sang Yun, Olincy, Ann, Olsen, Line, Van Os, Jim, Pantelis, Christos, Papadimitriou, George N., Papiol, Sergi, Parkhomenko, Elena, Pato, Michele T., Paunio, Tiina, Pejovic-Milovancevic, Milica, Perkins, Diana O., Pietiläinen, Olli, Pimm, Jonathan, Pocklington, Andrew J., Powell, John, Price, Alkes, Pulver, Ann E., Purcell, Shaun M., Quested, Digby, Rasmussen, Henrik B., Reichenberg, Abraham, Reimers, Mark A., Richards, Alexander L., Roffman, Joshua L., Roussos, Panos, Salomaa, Veikko, Sanders, Alan R., Schall, Ulrich, Schubert, Christian R., Schwab, Sibylle G., Scolnick, Edward M., Scott, Rodney J., Seidman, Larry J., Shi, Jianxin, Sigurdsson, Engilbert, Silagadze, Teimuraz, Silverman, Jeremy M., Sim, Kang, Slominsky, Petr, Smoller, Jordan W., So, Hon Cheong, Spencer, Chris C A, Stahl, Eli A., Stefansson, Hreinn, Steinberg, Stacy, Stogmann, Elisabeth, Straub, Richard E., Strengman, Eric, Scott Stroup, T., Subramaniam, Mythily, Suvisaari, Jaana, Svrakic, Dragan M., Szatkiewicz, Jin P., Söderman, Erik, Thirumalai, Srinivas, Toncheva, Draga, Tosato, Sarah, Veijola, Juha, Waddington, John, Walsh, Dermot, Wang, Dai, Wang, Qiang, Webb, Bradley T., Weiser, Mark, Wildenauer, Dieter B., Williams, Nigel M., Williams, Stephanie, Wolen, Aaron R., Wong, Emily H M, Wormley, Brandon K., Xi, Hualin Simon, Zai, Clement C., Zheng, Xuebin, Zimprich, Fritz, Wray, Naomi R., Stefansson, Kari, Visscher, Peter M., Adolfsson, Rolf, Andreassen, Ole A., Blackwood, Douglas H R, Bramon, Elvira, Buxbaum, Joseph D., Børglum, Anders D., Darvasi, Ariel, Domenici, Enrico, Ehrenreich, Hannelore, Esko, Tõnu, Gejman, Pablo V., Gill, Michael, Gurling, Hugh, Hultman, Christina M., Iwata, Nakao, Jablensky, Assen V., Jönsson, Erik G., Kendler, Kenneth S., Kirov, George, Knight, Jo, Lencz, Todd, Levinson, Douglas F., Li, Qingqin S., Liu, Jianjun, Malhotra, Anil K., McCarroll, Steven A., McQuillin, Andrew, Moran, Jennifer L., Mortensen, Preben B., Mowry, Bryan J., Ophoff, Roel A., Owen, Michael J., Palotie, Aarno, Pato, Carlos N., Petryshen, Tracey L., Posthuma, Danielle, Riley, Brien P., Sham, Pak C., Sklar, Pamela, Clair, David S., Weinberger, Daniel R., Wendland, Jens R., Werge, Thomas, Daly, Mark J., O'Donovan, Michael C., Sullivan, Patrick F., Keller, Matthew C., Biological Psychology, Johnson, Emma C, Bjelland, Douglas W, Howrigan, Daniel P, Abdellaoui, Abdel, Lee, S Hong, Keller, Matthew C, and Schizophrenia Working Group of the Psychiatric Genomics Consortium

Subjects
0301 basic medicine, Male, Cancer Research, Heredity, Ecology, Evolution, Behavior and Systematics, Molecular Biology, Genetics, Genetics (clinical), Social Sciences, Genome-wide association study, Disease, 030105 genetics & heredity, Runs of Homozygosity, Homozygosity, Consanguinity, Sociology, Polymorphism (computer science), Consortia, Medicine and Health Sciences, Genetics(clinical), Inbreeding, Ecology, Depression, Homozygote, Genomics, 3. Good health, Schizophrenia, Research Design, Physical Sciences, Female, Statistics (Mathematics), Research Article, lcsh:QH426-470, Evolution, Replication Studies, inbreeding, Single-nucleotide polymorphism, Biology, Genome Complexity, Research and Analysis Methods, Polymorphism, Single Nucleotide, 03 medical and health sciences, SDG 17 - Partnerships for the Goals, Behavior and Systematics, SDG 3 - Good Health and Well-being, Mental Health and Psychiatry, medicine, Confidence Intervals, Humans, replication study, Mood Disorders, Genome, Human, Biology and Life Sciences, Computational Biology, medicine.disease, schizophrenia, lcsh:Genetics, 030104 developmental biology, homozygosity, Mathematics, Genome-Wide Association Study
Abstract

It is well known that inbreeding increases the risk of recessive monogenic diseases, but it is less certain whether it contributes to the etiology of complex diseases such as schizophrenia. One way to estimate the effects of inbreeding is to examine the association between disease diagnosis and genome-wide autozygosity estimated using runs of homozygosity (ROH) in genome-wide single nucleotide polymorphism arrays. Using data for schizophrenia from the Psychiatric Genomics Consortium (n = 21,868), Keller et al. (2012) estimated that the odds of developing schizophrenia increased by approximately 17% for every additional percent of the genome that is autozygous (β = 16.1, CI(β) = [6.93, 25.7], Z = 3.44, p = 0.0006). Here we describe replication results from 22 independent schizophrenia case-control datasets from the Psychiatric Genomics Consortium (n = 39,830). Using the same ROH calling thresholds and procedures as Keller et al. (2012), we were unable to replicate the significant association between ROH burden and schizophrenia in the independent PGC phase II data, although the effect was in the predicted direction, and the combined (original + replication) dataset yielded an attenuated but significant relationship between Froh and schizophrenia (β = 4.86,CI(β) = [0.90,8.83],Z = 2.40,p = 0.02). Since Keller et al. (2012), several studies reported inconsistent association of ROH burden with complex traits, particularly in case-control data. These conflicting results might suggest that the effects of autozygosity are confounded by various factors, such as socioeconomic status, education, urbanicity, and religiosity, which may be associated with both real inbreeding and the outcome measures of interest., Author Summary It is well known that mating between relatives increases the risk that a child will have a rare recessive genetic disease, but there has also been increasing interest and inconsistent findings on whether inbreeding is a risk factor for common, complex psychiatric disorders such as schizophrenia. The best powered study to date investigating this theory predicted that the odds of developing schizophrenia increase by approximately 17% for every additional percent of the genome that shows evidence of inbreeding. In this replication, we used genome-wide single nucleotide polymorphism data from 18,562 schizophrenia cases and 21,268 controls to quantify the degree to which they were inbred and to test the hypothesis that schizophrenia cases show higher mean levels of inbreeding. Contrary to the original study, we did not find evidence for distant inbreeding to play a role in schizophrenia risk. There are various confounding factors that could explain the discrepancy in results from the original study and our replication, and this should serve as a cautionary note–careful attention should be paid to issues like ascertainment when using the data from genome-wide case-control association studies for secondary analyses for which the data may not have originally been intended.

Published
2016

5. No Reliable Association between Runs of Homozygosity and Schizophrenia in a Well-Powered Replication Study

Author

Stogmann, Elisabeth, Liang, Kung-Yee, Hoffman, Per, Herms, Stefan, Donohoe, Gary, Kalaydjieva, Luba, Waddington, John, Buckner, Randy L., Bevilacqua, Elizabeth, Mowry, Bryan J., Powell, John, Mattheisen, Manuel, Jablensky, Assen V., Dinan, Timothy, Kennedy, James L., Hammer, Christian, Stefansson, Kari, Fromer, Menachem, Mesholam-Gately, Raquelle I., Scott, Rodney J., Chong, Siow Ann, Milani, Lili, Wang, Dai, Stahl, Eli A., Agartz, Ingrid, Meijer, Carin J., Gopal, Srihari, Price, Alkes, Milanova, Vihra, Stahl, Eli, Farh, Kai-How, Murphy, Kieran C., Frank, Josef, Palotie, Aarno, Cohen, David, Bene, Judit, Slominsky, Petr, Seidman, Larry J., Demontis, Ditte, Olsen, Line, Giusti-Rodríguez, Paola, Pulver, Ann E., Andreassen, Ole A., Toncheva, Draga, Kuzelova-Ptackova, Hana, Knowles, James A., Sham, Pak C., Davis, Kenneth L., Strohmaier, Jana, Cormican, Paul, Bacanu, Silviu A., Nenadic, Igor, O'Donovan, Michael C., Haroutunian, Vahram, O'Dushlaine, Colm, Genovese, Giulio, Mortensen, Preben B., Friedl, Marion, Riley, Brien P., Chan, Raymond C.K., Wildenauer, Dieter B., Oh, Sang-Yun, Purcell, Shaun M., Cohen, Nadine, Stefansson, Hreinn, Ikeda, Masashi, Wendland, Jens R., Mattingsdal, Morten, Campion, Dominique, Magnusson, Patrik K.E., Gill, Michael, Albus, Margot, Nelis, Mari, Kucinskiene, Zita Ausrele, Crowley, James J., Li, Tao, Breen, Gerome, Franke, Lude, Thirumalai, Srinivas, Weinberger, Daniel R., Gejman, Pablo V., Quested, Digby, Dikeos, Dimitris, Olincy, Ann, Nicodemus, Kristin K., Keller, Matthew C., Owen, Michael J., Drapeau, Elodie, Visscher, Peter M., McIntosh, Andrew M., Straub, Richard E., Reimers, Mark A., Nertney, Deborah A., Buxbaum, Joseph D., Webb, Bradley T., Silverman, Jeremy M., Williams, Nigel M., Neale, Benjamin M., Hong Lee, Papadimitriou, George N., Laurent, Claudine, Lubinski, Jan, Robert Cloninger, Li, Miaoxin, Silagadze, Teimuraz, Amin, Farooq, Kahn, René S., Wong, Emily H. M., Buccola, Nancy G., Svrakic, Dragan M., Escott-Price, Valentina, Wang, Qiang, Schall, Ulrich, Clair, David S., Nisenbaum, Laura, Chee Keong, Jimmy Lee, Hansen, Mark, Malhotra, Anil K., Paunio, Tiina, Holmans, Peter A., Kim, Yunjung, Anthony O'Neill, Wray, Naomi R., Ruderfer, Douglas M., Nöthen, Markus M., Steinberg, Stacy, Chen, Eric Y.H., Macek, Milan, Freedman, Robert, Rujescu, Dan, Witt, Stephanie H., Farrell, Martilias S., Cheung, Eric F.C., Mallet, Jacques, Ripke, Stephan, Essioux, Laurent, Müller-Myhsok, Bertram, Heilmann-Heimbach, Stefanie, Abdellaoui, Abdel, Müller-Mhysok, Betram, Mors, Ole, Eichhammer, Peter, Knight, Jo, Levinson, Douglas F., Pantelis, Christos, Perkins, Diana O., Roussos, Panos, Neale, Benjamin, Schulze, Thomas G., Legge, Sophie E., Michie, Patricia T., Fanous, Ayman H., Julià, Antonio, Friedman, Joseph I., Zimprich, Fritz, Meier, Sandra, Murray, Robin M., Carrera, Noa, Van Os, Jim, Freimer, Nelson B., Blackwood, Douglas H. R., Parkhomenko, Elena, Sanders, Alan R., Kavanagh, David, Tosato, Sarah, Chambert, Kimberly D., Black, Donald W., Simonson, Matthew A., Rasmussen, Henrik B., Sullivan, Patrick F., Maher, Brion S., Gratten, Jacob, Ophoff, Roel A., Lencz, Todd, Kirov, George, Joa, Inge, Zai, Clement C., Spencer, Chris C.A., Limborska, Svetlana, Forstner, Andreas J., Godard, Stephanie, Hoffmann, Per, Shi, Jianxin, Khrunin, Andrey, Hofman, Andrea, Degenhardt, Franziska, Hultman, Christina M., Nikitina-Zake, Liene, Salomaa, Veikko, Lerer, Bernard, Myin-Germeys, Inez, Walters, James T.R., Petryshen, Tracey L., Nestadt, Gerald, Rietschel, Marcella, Adolfsson, Rolf, Konte, Bettina, Hirschhorn, Joel N., Subramaniam, Mythily, Wolen, Aaron R., Richards, Alexander L., Bulik-Sullivan, Brendan, Curtis, David, Scott Stroup, Wormley, Brandon K., Pocklington, Andrew J., Karjalainen, Juha, Melle, Ingrid, Jönsson, Erik G., Reichenberg, Abraham, Kähler, Anna K., Bjelland, Douglas W., Domenici, Enrico, Huang, Hailiang, McDonald, Colm, Collier, David A., Cheng, Wei, Bramon, Elvira, Posthuma, Danielle, Söderman, Erik, Alexander, Madeline, Bruggeman, Richard, Moran, Jennifer L., Xi, Hualin Simon, Djurovic, Srdjan, Darvasi, Ariel, Sigurdsson, Engilbert, Hougaard, David M., O’Dushlaine, Colm, Williams, Stephanie, Cichon, Sven, Walsh, Dermot, Dudbridge, Frank, Ehrenreich, Hannelore, Liu, Jianjun, Pato, Michele T., Mokrab, Younes, Lee, Phil, Begemann, Martin, Iwata, Nakao, Kucinskas, Vaidutis, de Haan, Lieuwe, Hollegaard, Mads V., Suvisaari, Jaana, Werge, Thomas, McCarroll, Steven A., Howrigan, Daniel P., Esko, Tõnu, Nordin, Annelie, Pimm, Jonathan, Golimbet, Vera, Corvin, Aiden, Hartmann, Annette M., Byerley, William, Li, Qingqin S., Johnson, Emma C., Veijola, Juha, Craddock, Nick, Strengman, Eric, Weiser, Mark, Bergen, Sarah E., Gurling, Hugh, Eriksson, Johan, McCarley, Robert W., Schwab, Sibylle G., Schubert, Christian R., Pejovic-Milovancevic, Milica, Lieberman, Jeffrey, Maier, Wolfgang, Goldstein, Jacqueline I., Bigdeli, Tim B., Pers, Tune H., Marsal, Sara, Agerbo, Esben, Cantor, Rita M., Melegh, Bela, Lönnqvist, Jouko, Daly, Mark J., Cai, Guiqing, Duan, Jubao, Smoller, Jordan W., Sklar, Pamela, Papiol, Sergi, Loughland, Carmel M., Hamshere, Marian L., Giegling, Ina, Cahn, Wiepke, Catts, Stanley V., Zheng, Xuebin, Carr, Vaughan J., Børglum, Anders D., Roffman, Joshua L., Hansen, Thomas, Sim, Kang, Belliveau, Richard A., Morris, Derek W., Pietiläinen, Olli, Metspalu, Andres, Durmishi, Naser, Karachanak-Yankova, Sena, Del Favero, Jurgen, So, Hon-Cheong, Klovins, Janis, Scolnick, Edward M., Davidson, Michael, Henskens, Frans A., Mowry, Bryan, Chen, Ronald Y.L., Georgieva, Lyudmila, Szatkiewicz, Jin P., McQuillin, Andrew, Kendler, Kenneth S., O'Callaghan, Eadbhard, Borglum, Anders, and Pato, Carlos N.

Subjects
3. Good health
Abstract

It is well known that inbreeding increases the risk of recessive monogenic diseases, but it is less certain whether it contributes to the etiology of complex diseases such as schizophrenia. One way to estimate the effects of inbreeding is to examine the association between disease diagnosis and genome-wide autozygosity estimated using runs of homozygosity (ROH) in genome-wide single nucleotide polymorphism arrays. Using data for schizophrenia from the Psychiatric Genomics Consortium (n = 21,868), Keller et al. (2012) estimated that the odds of developing schizophrenia increased by approximately 17% for every additional percent of the genome that is autozygous (β = 16.1, CI(β) = [6.93, 25.7], Z = 3.44, p = 0.0006). Here we describe replication results from 22 independent schizophrenia case-control datasets from the Psychiatric Genomics Consortium (n = 39,830). Using the same ROH calling thresholds and procedures as Keller et al. (2012), we were unable to replicate the significant association between ROH burden and schizophrenia in the independent PGC phase II data, although the effect was in the predicted direction, and the combined (original + replication) dataset yielded an attenuated but significant relationship between Froh and schizophrenia (β = 4.86,CI(β) = [0.90,8.83],Z = 2.40,p = 0.02). Since Keller et al. (2012), several studies reported inconsistent association of ROH burden with complex traits, particularly in case-control data. These conflicting results might suggest that the effects of autozygosity are confounded by various factors, such as socioeconomic status, education, urbanicity, and religiosity, which may be associated with both real inbreeding and the outcome measures of interest.

6. Narrow-sense heritability estimation of complex traits using identity-by-descent information.

Author

Evans LM, Tahmasbi R, Jones M, Vrieze SI, Abecasis GR, Das S, Bjelland DW, de Candia TR, Yang J, Goddard ME, Visscher PM, and Keller MC

Subjects
Gene Frequency, Genome, Human, Haplotypes, Humans, Phenotype, Polymorphism, Single Nucleotide, Chromosomes, Human
Abstract

Heritability is a fundamental parameter in genetics. Traditional estimates based on family or twin studies can be biased due to shared environmental or non-additive genetic variance. Alternatively, those based on genotyped or imputed variants typically underestimate narrow-sense heritability contributed by rare or otherwise poorly tagged causal variants. Identical-by-descent (IBD) segments of the genome share all variants between pairs of chromosomes except new mutations that have arisen since the last common ancestor. Therefore, relating phenotypic similarity to degree of IBD sharing among classically unrelated individuals is an appealing approach to estimating the near full additive genetic variance while possibly avoiding biases that can occur when modeling close relatives. We applied an IBD-based approach (GREML-IBD) to estimate heritability in unrelated individuals using phenotypic simulation with thousands of whole-genome sequences across a range of stratification, polygenicity levels, and the minor allele frequencies of causal variants (CVs). In simulations, the IBD-based approach produced unbiased heritability estimates, even when CVs were extremely rare, although precision was low. However, population stratification and non-genetic familial environmental effects shared across generations led to strong biases in IBD-based heritability. We used data on two traits in ~120,000 people from the UK Biobank to demonstrate that, depending on the trait and possible confounding environmental effects, GREML-IBD can be applied to very large genetic datasets to infer the contribution of very rare variants lost using other methods. However, we observed apparent biases in these real data, suggesting that more work may be required to understand and mitigate factors that influence IBD-based heritability estimates.

Published
2018
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