Luteolin promotes neuronogenesis in hippocampus of chronic unpredictable mild stress rats and primary hippocampus of fetal rats

doi:10.19852/j.cnki.jtcm.20240626.002

Journal of Traditional Chinese Medicine ›› 2024, Vol. 44 ›› Issue (4): 670-679.DOI: 10.19852/j.cnki.jtcm.20240626.002

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Luteolin promotes neuronogenesis in hippocampus of chronic unpredictable mild stress rats and primary hippocampus of fetal rats

LIU Tongtong¹, ZHANG Xi², YANG Hui³, LIN Xiaoyuan³, LIU Jian³, ZHANG Xiuli¹, GUO Dongwei², ZHAO Hongqing¹, ZOU Manshu¹, LEI Chang¹, LONG Hongping³, LUO Yan¹, XIANG Yun¹, GE Jinwen⁴, WANG Yuhong¹, MENG Pan¹()

1 Institute of Innovation and Applied Research in Chinese Medicine, Hunan University of Chinese Medicine, Changsha 410208, China
2 the Second People's Hospital of Hunan Province, Changsha 410007, China
3 The First Affiliated Hospital, Hunan University of Chinese Medicine, Changsha 410007, China
4 Hunan Academy of Chinese Medicine, Changsha 410013, China

Received:2023-01-12 Accepted:2023-08-22 Online:2024-08-15 Published:2024-06-26
Contact: MENG Pan, Institute of Innovation and Applied Research in Chinese Medicine, Hunan University of Chinese Medicine, Changsha 410208, China. mengpan@hnucm.edu.cn Telephone: +86-15873153921
Supported by:
Outstanding Youth Project of Natural Science Foundation of Hunan Province: Mechanisms of Emotional-behavioural and Cognitive Impairment in Depression and Intervention with Traditional Chinese Medicine(2020JJ3027);Training Plan of Outstanding Innovative Youth of Changsha(kq2009018);Key Projects of Hunan Provincial Department of Education: Hspa5/PrPc-based Study on the Mechanism of Lymphoid System Damage in Cerebral Small Vessel Disease with Depression and Intervention with Traditional Chinese Medicine(23A0281);Traditional Chinese Medicine Research Program Project of Hunan Province: Mechanisms of Impairment of Ventral and Dorsal Hippocampal Differential Function in Depression based on Sonic Hedgehog/Brain-Derived Neurotrophic Factor Signalling-Mediated Synaptogenesis in Newborn Neurons and Intervention with Traditional Chinese Medicine(B2023021);Open Fund Project of State Key Laboratory of Traditional Chinese Medicine Powder and Innovative Drugs: Mechanisms of Glymphatic Iinjury in Cerebral Small Vessel Disease with Depression Based on Aquaporin Protein-4 Signalling-Mediated Astrocyte-Responsive Hyperplasia and Intervention with Traditional Chinese Medicine(23PTKF1013)

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Abstract

Abstract:

OBJECTIVE: To investigate the effects of luteolin on chronic unpredictable mild stress (CUMS)-induced depressive rats and corticosterone (CORT)-induced depressive primary hippocampal neurons, and to elucidate the mechanism behind the action.

METHODS: The antidepressant mechanism of luteolin was studied by using CUMS rat model and primary hippocampal neurons in fetal rats. In vivo, novelty suppressed feeding, open-field and sucrose preference tests as well as Morris water maze were evaluated. The content of brain derived neurotrophic factor (BDNF), 5-hydroxytryptamine (5-HT), norepinephrine (NE), and dopamine (DA) in serum were detected by enzyme-linked immunosorbent assay. The mechanisms of luteolin were explored based on neurotrophin and hippocampal neurogenesis, and proliferation. Survival of the septo-temporal axis in hippocampus was assayed using the 5-bromo-2-deoxyuridine (BrdU), the expression of BDNF, neurotrophin-3 (NT-3), and nerve growth factor (NGF) in hippocampus dentate gyrus region were measured by Western-blotting. In vitro, BDNF, NT-3, tropomyosin receptor kinase B (TrkB), and phosphorylated cyclic adenosine monophosphate responsive element binding protein (p-CREB) were detected through the high content analysis (HCA) to investigate neurotrophin and apoptosis.

RESULTS: Induction of CUMS in rats induced depressive symptoms, while luteolin significantly enhanced sucrose consumption, decreased feeding latency, increased locomotor activity, escape latency, distance of target quadrant and regulated the content of depressive-like biomarkers. Histology analysis revealed that luteolin increased the abundance of new born neurons that had been labeled with BrdU, BrdU + neuronal nuclear antigen, and BrdU + doublecortin in septo-temporal axis of S2 (mid-septal) and T3 (mid-temporal). Moreover, expression of BDNF, NT-3, and NGF increased significantly in the septo-temporal axis of S2 and T3. HCA showed increased expression of BDNF, NT-3, TrkB and p-CREB in primary hippocampal neurons.

CONCLUSION: The results provided direct evidence that luteolin has an antidepressant effect and could effectively promote the regeneration of the septotemporal axis nerve and hippocampal neuronutrition, which suggested that the antidepressant effect of luteolin may be related to hippocampal neurogenesis.

Key words: luteolin, depression, chronic unpredicted mild stress, hippocampal neurogenesis, septo-temporal axis

LIU Tongtong, ZHANG Xi, YANG Hui, LIN Xiaoyuan, LIU Jian, ZHANG Xiuli, GUO Dongwei, ZHAO Hongqing, ZOU Manshu, LEI Chang, LONG Hongping, LUO Yan, XIANG Yun, GE Jinwen, WANG Yuhong, MENG Pan. Luteolin promotes neuronogenesis in hippocampus of chronic unpredictable mild stress rats and primary hippocampus of fetal rats[J]. Journal of Traditional Chinese Medicine, 2024, 44(4): 670-679.

Figures/Tables 10

Table 1 Behavior scores in each group

Group	n	Open field		Latency to feed (s)	Sugar preference (%)
Group	n	Horizontal	Vertical	Latency to feed (s)	Sugar preference (%)
Control	8	114.5±9.4	9.6±1.6	10.6±10.6	77.2±3.5
CUMS	8	10.0±2.7^a	1.7±0.5^a	90.7±19.4^a	28.1±3.6^a
Luteolin-H	8	97.6±19.1^b	7.9±1.7^b	7.2±4.0^b	70.9±3.0^b
Luteolin-L	8	16.1±1.7	4.4±1.3	45.4±14.6	36.1±2.2
Fluoxetine	8	77.4±7.0^b	6.9±0.9^b	10.9±7.4^b	68.7±3.2^b

Table 2 Body weight in each group (g)

Group	n	1 week	2 weeks	3 weeks	4 weeks
Control	8	214.1±2.5	274.2±3.3	333.0±5.1	404.5±5.4
CUMS	8	217.5±2.5	240.1±4.6^a	272.6±4.7^a	301.5±3.8^a
Luteolin-H	8	209.2±4.1	247.8±2.7	290.6±4.8^b	346.4±7.0^c
Luteolin-L	8	216.9±3.4	241.6±4.8	280.6±6.2	310.1±10.5
Fluoxetine	8	215.9±4.4	244.9±6.1	301.8±9.3^c	342.8±4.1^c

Figure 1 Escape latency and crossing distance of the platform position in each group A: the results of Morris Water maze test of each group; B: trace plot of escape latency of control (B1), CUMS (B2), luteolin-H (B3), luteolin-L (B4), fluoxetine (B5) groups.; C: trace plot of Crossing distance of the platform position of control (C1), CUMS (C2), luteolin-H (C3), luteolin-L (C4), fluoxetine (C5) groups. Control: unstressed and intragastrically given 2 mL distilled water daily. CUMS: were intragastrically with distilled water. Luteolin-H: were intragastrically with luteolin at 20 mg·kg-1·d-1. Luteolin-L: were intragastrically with luteolin at 10 mg·kg-1·d-1. Fluoxetine: were intragastrically with fluoxetine at 5.4 mg·kg-1·d-1. CUMS: chronic unpredictable mild stress. Statistical significance among groups was conducted using one-way analysis of variance. Data were presented as mean ± standard error of mean (n = 8). aP < 0.0,1 compared with the control group; bP < 0.05, cP < 0.01, compared with the CUMS group.

Table 3 Content of BDNF, 5-HT, NE and DA in serum in each group (ng/mL)

Group	n	BDNF	5-HT	NE	DA
Control	8	38.3±1.9	75.8±2.0	22.5±1.1	45.2±0.8
CUMS	8	17.5±0.7^a	35.6±3.0^a	13.2±0.7^a	20.5±0.3^a
Luteolin-H	8	32.6±1.9^b	63.5±4.9^b	22.9±1.2^b	45.3±0.6^b
Luteolin-L	8	19.4±0.8	46.8±3.2^c	13.9±0.8	19.9±0.2
Fluoxetine	8	33.9±2.1^b	65.2±4.3^d	24.4±1.0^b	45.8±0.7^b

Figure 2 Expression of BDNF, NT-3, NGF in the dentate gyrus of hippocampus A: gray value of BDNF; B: gray value of NT-3; C: gray value of NGF. Control: unstressed and intragastrically given 2 mL distilled water daily. CUMS: were intragastrically with distilled water. Luteolin-H: were intragastrically with luteolin at 20 mg·kg-1·d-1. Luteolin-L: were intragastrically with luteolin at 10 mg·kg-1·d-1. Fluoxetine: were intragastrically with fluoxetine at 5.4 mg·kg-1·d-1. CUMS: chronic unpredictable mild stress; BDNF: brain derived neurotrophic factor; NT-3: neurotrophin-3; NGF: nerve growth factor. Statistical significance among groups was conducted using one-way analysis of variance. Data are expressed as mean ± standard error of mean (n = 3). aP < 0.01, compared with the control group; bP < 0.01, compared with the CUMS group.

Figure 3 Neuronal differentiation and migration along the septo-temporal axis of hippocampus in each group Magnification of pictures is 100 ×. A: Representative pictures of BrdU+/NeuN+ cells. A1: expression of BrdU in the S1; A2: expression of NeuN in the S1; A3: expression of DAPI in the S1; A4: merged expression of BrdU, NeuN, and DAPI in the S1; A5: expression of BrdU in the S2; A6: expression of NeuN in the S2; A7: expression of DAPI in the S2; A8: merged expression of BrdU, NeuN, and DAPI in the S2; A9: expression of BrdU in the T3; A10: expression of NeuN in the T3; A11: expression of DAPI in the T3; A12: merged expression of BrdU, NeuN, and DAPI in the T3; A13: expression of BrdU in the T4; A14: expression of NeuN in the T4; A15: expression of DAPI in the T4; A16: merged expression of BrdU, NeuN, and DAPI in the T4; B: BrdU+/ NeuN+ cells per mm3. C: representative pictures of BrdU+/ DCX+ cells. C1: expression of BrdU in the S1; C2: expression of DCX in the S1; C3: expression of DAPI in the S1; C4: merged expression of BrdU, DCX, and DAPI in the S1; C5: expression of BrdU in the S2; C6: expression of DCX in the S2; C7: expression of DAPI in the S2; C8: merged expression of BrdU, DCX, and DAPI in the S2; C9: expression of BrdU in the T3; C10: expression of DCX in the T3; C11: expression of DAPI in the T3; C12: merged expression of BrdU, DCX, and DAPI in the T3; C13: expression of BrdU in the T4; C14: expression of DCX in the T4; C15: expression of DAPI in the T4; C16: merged expression of BrdU, DCX, and DAPI in the T4; D: BrdU+/ DCX+ cells per mm3. Control: unstressed and intragastrically given 2 mL distilled water daily. CUMS: were intragastrically with distilled water. Luteolin-H: were intragastrically with luteolin at 20 mg·kg-1·d-1. Luteolin-L: were intragastrically with luteolin at 10 mg·kg-1·d-1. Fluoxetine: were intragastrically with fluoxetine at 5.4 mg·kg-1·d-1. CUMS: chronic unpredictable mild stress; BrdU: 5-bromo-2-deoxyuridine; DAPI: 4’,6-Diamidino-2’-phenylindole; NeuN: Neuron specific nuclear protein antigen; DCX: doublecortin; S1: septal; S2: mid-septal; T3: mid-temporal; T4: temporal. Statistical significance among groups was conducted using one-way analysis of variance. Data were shown as mean ± standard error of mean (n = 3). aP < 0.01, dP < 0.05, compared with the control group; bP < 0.05, cP < 0.01, compared with the CUMS group.

Table 4 Expression of BDNF along the septo-temporal axis of hippocampus in the indicated groups

Group	n	Average fluorescence intensity of BDNF
Group	n	S1	S2	T3	T4
Control	8	0.403±0.023	0.600±0.023	0.577±0.023	0.233±0.022
CUMS	8	0.273±0.023^a	0.297±0.020^c	0.213±0.032^c	0.117±0.018^a
Luteolin-H	8	0.383±0.020^b	0.507±0.018^d	0.440±0.021^d	0.190±0.012
Luteolin-L	8	0.217±0.015	0.337±0.026	0.277±0.027	0.153±0.015
Fluoxetine	8	0.403±0.030^b	0.540±0.044^d	0.477±0.023^d	0.183±0.019

Table 5 Expression of NT-3 along the septo-temporal axis of hippocampus in the indicated groups

Group	n	S1	S2	T3	T4
Control	8	0.450±0.012	0.593±0.026	0.553±0.020	0.280±0.017
CUMS	8	0.183±0.020^a	0.293±0.015^a	0.207±0.029^a	0.197±0.018^d
Luteolin-H	8	0.277±0.020^b	0.493±0.015^c	0.493±0.026^c	0.213±0.015
Luteolin-L	8	0.227±0.015	0.313±0.020	0.327±0.035	0.203±0.015
Fluoxetine	8	0.290±0.012^b	0.507±0.035^c	0.463±0.026^c	0.273±0.026

Table 6 Expression of NGF along the septo-temporal axis of hippocampus in the indicated groups

Group	n	Average fluorescence intensity of NGF
Group	n	S1	S2	T3	T4
Control	8	0.447±0.020	0.550±0.023	0.523±0.015	0.297±0.020
CUMS	8	0.237±0.018^a	0.277±0.020^a	0.293±0.032^a	0.197±0.018^a
Luteolin-H	8	0.277±0.018	0.493±0.015^b	0.490±0.015^b	0.263±0.026
Luteolin-L	8	0.263±0.009	0.343±0.020	0.327±0.035	0.223±0.015
Fluoxetine	8	0.317±0.015	0.540±0.038^b	0.487±0.023^b	0.283±0.026

Figure 4 Expression of BDNF, NT-3, TrkB, and p-CREB in primary cells in the indicated groups Magnification of pictures is ×400. A: relative integrated density of BDNF; B: relative integrated density of NT-3; C: relative integrated density of TrkB; D: relative integrated density of p-CREB. Control: unstressed and intragastrically given 2 mL distilled water daily. CUMS: were intragastrically with distilled water. Luteolin-H: were intragastrically with luteolin at 20 mg·kg-1·d-1. Luteolin-L: were intragastrically with luteolin at 10 mg·kg-1·d-1. Fluoxetine: were intragastrically with fluoxetine at 5.4 mg·kg-1·d-1. CUMS: chronic unpredictable mild stress; BDNF: brain derived neurotrophic factor; NT-3: neurotrophin-3; TrkB: tropomyosin receptor kinase B; p-CREB: phosphorylated cAMP responsive element binding protein. Statistical significance among groups was conducted using one-way analysis of variance. Data were shown as mean ± standard error of mean (n = 3). aP < 0.01, dP < 0.05, compared with the control group; bP < 0.01, cP < 0.05, compared with the CUMS group.

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Luteolin promotes neuronogenesis in hippocampus of chronic unpredictable mild stress rats and primary hippocampus of fetal rats

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