Mutants of the white ABCG Transporter in Drosophila melanogaster Have Deficient Olfactory Learning and Cholesterol Homeostasis

Myers, Jennifer L.; Porter, Maria; Narwold, Nicholas; Bhat, Krishna; Dauwalder, Brigitte; Roman, Gregg

doi:10.3390/ijms222312967

Open AccessArticle

Mutants of the white ABCG Transporter in Drosophila melanogaster Have Deficient Olfactory Learning and Cholesterol Homeostasis

by

Jennifer L. Myers

¹,

Maria Porter

²,

Nicholas Narwold

³,

Krishna Bhat

³,

Brigitte Dauwalder

¹ and

Gregg Roman

^4,*

¹

Department of Biology and Biochemistry, University of Houston, Houston, TX 77096, USA

²

Department of Biology, University of Mississippi, Oxford, MS 38677, USA

³

Department of Molecular Medicine, University of Southern Florida, Tampa, FL 33613, USA

⁴

Department of Biomolecular Sciences, University of Mississippi, Oxford, MS 38677, USA

^*

Author to whom correspondence should be addressed.

Int. J. Mol. Sci. 2021, 22(23), 12967; https://doi.org/10.3390/ijms222312967

Submission received: 11 October 2021 / Revised: 19 November 2021 / Accepted: 26 November 2021 / Published: 30 November 2021

(This article belongs to the Special Issue Molecular Mechanisms Employed by Neurons to Receive and Transduce Signals Essential for Learning and Memory)

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Abstract

Drosophila’s white gene encodes an ATP-binding cassette G-subfamily (ABCG) half-transporter. White is closely related to mammalian ABCG family members that function in cholesterol efflux. Mutants of white have several behavioral phenotypes that are independent of visual defects. This study characterizes a novel defect of white mutants in the acquisition of olfactory memory using the aversive olfactory conditioning paradigm. The w¹¹¹⁸ mutants learned slower than wildtype controls, yet with additional training, they reached wildtype levels of performance. The w¹¹¹⁸ learning phenotype is also found in the w^apricot and w^coral alleles, is dominant, and is rescued by genomic white and mini-white transgenes. Reducing dietary cholesterol strongly impaired olfactory learning for wildtype controls, while w¹¹¹⁸ mutants were resistant to this deficit. The w¹¹¹⁸ mutants displayed higher levels of cholesterol and cholesterol esters than wildtype under this low-cholesterol diet. Increasing levels of serotonin, dopamine, or both in the white mutants significantly improved w¹¹¹⁸ learning. However, serotonin levels were not lower in the heads of the w¹¹¹⁸ mutants than in wildtype controls. There were also no significant differences found in synapse numbers within the w¹¹¹⁸ brain. We propose that the w¹¹¹⁸ learning defect may be due to inefficient biogenic amine signaling brought about by altered cholesterol homeostasis.

Keywords: olfactory learning; white; Drosophila; cholesterol; serotonin; dopamine; ABCG transporter; freeze tolerance

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MDPI and ACS Style

Myers, J.L.; Porter, M.; Narwold, N.; Bhat, K.; Dauwalder, B.; Roman, G. Mutants of the white ABCG Transporter in Drosophila melanogaster Have Deficient Olfactory Learning and Cholesterol Homeostasis. Int. J. Mol. Sci. 2021, 22, 12967. https://doi.org/10.3390/ijms222312967

AMA Style

Myers JL, Porter M, Narwold N, Bhat K, Dauwalder B, Roman G. Mutants of the white ABCG Transporter in Drosophila melanogaster Have Deficient Olfactory Learning and Cholesterol Homeostasis. International Journal of Molecular Sciences. 2021; 22(23):12967. https://doi.org/10.3390/ijms222312967

Chicago/Turabian Style

Myers, Jennifer L., Maria Porter, Nicholas Narwold, Krishna Bhat, Brigitte Dauwalder, and Gregg Roman. 2021. "Mutants of the white ABCG Transporter in Drosophila melanogaster Have Deficient Olfactory Learning and Cholesterol Homeostasis" International Journal of Molecular Sciences 22, no. 23: 12967. https://doi.org/10.3390/ijms222312967

APA Style

Myers, J. L., Porter, M., Narwold, N., Bhat, K., Dauwalder, B., & Roman, G. (2021). Mutants of the white ABCG Transporter in Drosophila melanogaster Have Deficient Olfactory Learning and Cholesterol Homeostasis. International Journal of Molecular Sciences, 22(23), 12967. https://doi.org/10.3390/ijms222312967

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Mutants of the white ABCG Transporter in Drosophila melanogaster Have Deficient Olfactory Learning and Cholesterol Homeostasis

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