The bioprospecting potential of <i>Clusia fluminensis</i> Planch. &amp; Triana: a scoping review

FARIA, GISELLE M.; LEMOS, ANA PATRICIA A.; ANHOLETI, MARIA C.; PAIVA, SELMA R.; AMORIM, LIDIA M.F.

doi:10.1590/0001-3765202320211605

GISELLE M. FARIA

search and selection of the papers, categorization by bibliographic databases, writing of original draft, data analysis and organization of the results

Universidade Federal Fluminense, Instituto de Biologia, Departamento de Biologia Celular e Molecular, Rua Prof. Marcos Waldemar de Freitas Reis, Bloco M, 311, São Domingos, 24210-201 Niterói, RJ, Brazil

https://orcid.org/0000-0002-4287-1651

ANA PATRICIA A. LEMOS

search and selection of the papers, categorization by bibliographic databases, figures design

Universidade Federal Fluminense, Instituto de Biologia, Departamento de Biologia Celular e Molecular, Rua Prof. Marcos Waldemar de Freitas Reis, Bloco M, 311, São Domingos, 24210-201 Niterói, RJ, Brazil

https://orcid.org/0000-0002-4119-9656

MARIA C. ANHOLETI

reviewing and editing

Universidade Federal Fluminense, Faculdade de Farmácia, Departamento de Farmácia e Administração Farmacêutica, Rua Dr. Mario Vianna, 523, Santa Rosa, 24241-001 Niterói, RJ, Brazil

https://orcid.org/0000-0003-1552-9161

SELMA R. PAIVA

reviewing and editing, project administration, funding acquisition

Universidade Federal Fluminense, Instituto de Biologia, Departamento de Biologia Geral, Rua Prof. Marcos Waldemar de Freitas Reis, Bloco M, 111, São Domingos, 24210-201 Niterói, RJ, Brazil

Programa de Pós-Graduação em Ciências Aplicadas a Produtos para Saúde, Universidade Federal Fluminense, Faculdade de Farmácia, Rua Dr. Mario Vianna, 523, Santa Rosa, 24241-001 Niterói, RJ, Brazil

https://orcid.org/0000-0002-8295-7011

LIDIA M.F. AMORIM

conceptualization, reviewing and editing, data analysis, supervision, project administration, funding acquisition

Universidade Federal Fluminense, Instituto de Biologia, Departamento de Biologia Celular e Molecular, Rua Prof. Marcos Waldemar de Freitas Reis, Bloco M, 311, São Domingos, 24210-201 Niterói, RJ, Brazil

https://orcid.org/0000-0001-7282-9748

Correspondence to: Lídia Amorim E-mail: amorimlidia@id.uff.br

Figures (2)
Tables (3)

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Figure 1
Flow diagram of literature search results and its critical appraisal. The flowchart a) shows the steps adopted on records selection. The superpositions of the captured records from four databases are depicted in diagram b). The critical appraisal (CA; H: high, M: moderate) of the selected studies according to the main research field (1: Phytochemistry, 2: Bioactivity) is shown in c).

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Figure 2
Antibothropic activity of Clusia fluminensis extracts assayed in vitro and in vivo. a) In vitro assays were performed in which the venoms of Bothrops jararaca or B. jararacussu were pre-incubated with plant extracts or isolated molecules and then with: (i) azocasein, (ii) plasma or (iii) a mixture of human red blood cells and hen’s egg yolk emulsion to determine, respectively (i) proteolytic inhibition, (ii) clotting time and (iii) antihemolytic activity. Hemolysis induced by the venom of B. jararacussu was not tested, since this venom has low hemolytic activity. b) In vivo antibothropic evaluation was performed using pre-incubation, treatment or prevention protocols using distinct routes of administration (*). As with the in vitro assays, in the in vivo incubation protocol, venom was pre-incubated with the plant extracts before injection in mice. For the treatment protocol, the mice were pre-injected with venom and then treated with each extract. For the prevention protocol, mice were fed with the extracts before the venom injection. Distinct routes of administration for snake venoms and plant extracts were as follows: top (topical), p.o. (oral), s.c. (subcutaneous), i.v. (intravenous), i.m. (intramuscular), i.p. (intraperitoneal), i.d. (intradermal). Positive control groups received snake venom mixed with saline, and negative controls received plant extracts alone. Myotoxicity assay was only performed for B. jararacussu envenomation, due to its marked effect compared to B. jararaca.

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Table I
Clusia fluminensis phytochemical profile.

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Table II
Overview of the biological activity of Clusia fluminensis extracts and isolated compounds.

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Table III
Anti-Bothrops snake venom activity of organic and aqueous extracts of Clusia fluminensis.

Reference	Plant Organ	Solvent used on Extraction	Chemical Class *	Compound	Content	Unit	Identification / Quantification method **
Guimarães et al. (2021)GUIMARÃES A, VIEIRA R & VIEIRA A. 2021. Structure of leaf galls in Clusia fluminensis Planch. and Triana (Clusiaceae): sex-biased development in a dioecious host plant. Plants 10: 1-19.	Leaves	Methanol	Total phenolics	-	16.29 ± 0.66 (pistillate individuals)	mg/g	Spectrophotometry (760 nm)
			Total phenolics	-	10.15 ± 0.31 (staminate individuals)	mg/g	Spectrophotometry (760 nm)
			Flavonoids	-	7.54 ± 0.09 (pistillate individuals)	mg/g	Spectrophotometry (760 nm)
			Flavonoids	-	6.75 ± 0.04 (staminate individuals)	mg/g	Spectrophotometry (760 nm)
Mazza et al. (2019)MAZZA KEL, SANTIAGO MCPA, PACHECO S, NASCIMENTO LSM, BRAGA ECO, MARTINS VC, CUNHA CP, GODOY RLO & BORGUINI RG. 2019. Determination of bioactive compounds in Clusia fluminensis Planch. & Triana fruit’s arils. Rev Virtual Química 11: 3-17.	Arils of the fruits with seeds	Sulfuric acid 0.05 M	Vitamin (^a)	Ascorbic acid	3.77 ± 0.82	mg/100 g	HPLC (ion exchange chromatography) / Spectrophotometry (242.6 nm)
		Methanol : Acetic Acid	Phenolic acids (^b)	Protocatechuic acid	115.14 ± 58.23	µg / g	HPLC-DAD (C18) / Spectrophotometry (270 - 310 nm)
				p-hydroxybenzoic acid	11.43 ± 0.32	µg / g
				p-hydroxycinnamic acid	5.97 ± 0.41	µg / g
		Methanol : Acetic Acid and alkaline or acid hydrolysis	Total phenolic acids (^b)	Protocatechuic acid	55.82 ± 12.23	µg / g
				p-hydroxybenzoic acid	16.76 ± 1.06	µg / g
				p-hydroxycinnamic acid	49.03 ± 12.69	µg / g
		Methanol : H₂O	Flavonoids (^c)	Rhamnetin and rhamnetin derivative	-		HPLC-DAD (C18) / Spectrophotometry (270 - 310 nm)
		Acetone : Petroleum ether	Carotenoids (^d)	Zeaxanthin	823	µg / g	HPLC UV-VIS / Spectrophotometry (450 nm)
				β-cryptoxanthin	-
				Lutein	-
Camara et al. (2018)CAMARA CAGD, MARSAIOLI AJ & BITTRICH V. 2018. Chemical constituents of apolar fractions from fruit latex of twelve Clusia species (Clusiaceae). An Acad Bras Cienc 90: 1919-1927.	Fruit latex	Methanolic latex collection from fresh cut fruits	Fatty acid derivative	Tetradecane	7.82	%	GC - FID / GC - MS
			Terpenoids	α-copaene	8.69	%	GC - FID / GC - MS
				β-caryophyllene	35.61	%
				α-humulene	2.11	%
				Germacrene D	8.78	%
				β-selinene	12.44	%
				α-selinene	6.56	%
				trans-β-guaiene	2.18	%
				Spathulenol	6.37	%
				Caryophyllene Oxide	3.45	%
				10-epi-γ-eudesmol	5.54	%
			Benzenoids	p-anysaldehyde	0.36	%	GC - FID / GC - MS
			Benzenoids	Acetophenone	traces	-	GC - FID / GC - MS
Anholeti et al. (2017)ANHOLETI MC, SILVA KMM, MORAES MG, SANTOS MG, FIGUEIREDO MR, KAPLAN MAC, JOFFILY A & PAIVA SR. 2017. Leaf anatomy and epicuticular waxes composition of Clusia fluminensis Planch. & Triana (Clusiaceae). Arab J Med Aromat Plants 55: 68-86.	Leaves wax	Chloroform	Terpenoids	Epifriedelinol	23.98 to 70	%	GC-MS
				Friedelin	58.37	%
				α a- β amyrin	-	-
				Lupenone	-	-
			Steroids	Sitosterol	-	-	GC-MS
			Steroids	Stigmasterol	-	-	GC-MS
Duprat et al. (2017)DUPRAT RC ET AL. 2017. Laboratory evaluation of Clusia fluminensis extracts and their isolated compounds against Dysdercus peruvianus and Oncopeltus fasciatus. Rev Bras Farmacogn 27: 59-66.	Fruit	Hexane	Terpenoids	Lanosterol	40.6	%	GC - MS
			Terpenoids	Lanosterol isomers	10.73	%	GC - MS
			Fatty acids	Palmitic acid	-	-	GC - MS
			Fatty acids	Oleic acid	-	-	GC - MS
Anholeti et al. (2015)ANHOLETI MC, DUPRAT RC, FIGUEIREDO MR, KAPLAN MAC, SANTOS MG, GONZALEZ MS, RATCLIFFE NA, FEDER D, PAIVA SR & MELLO CB. 2015. Biocontrol evaluation of extracts and a major component, clusianone, from Clusia fluminensis Planch. & Triana against Aedes aegypti. Mem Inst Oswaldo Cruz 110: 629-635.	Flower	Hexane	Polyisoprenylated benzophenone	Clusianone tautomeric pair	54.85	%	GC-MS
	Flower	Hexane	Terpenoid	Lanosterol	9.74	%	GC-MS
Meneses et al. (2015)MENESES LC, RIBEIRO MS, ANHOLETI MC, FIGUEIREDO MR, KAPLAN MAC, SANTOS MG, PEREIRA HS, PAIVA SR & PAIXÃO ICNP. 2015. Cytotoxicity and antiviral activity of extracts and compounds isolated from Clusia fluminensis. DST - J Bras Doenças Sex Transm 27: 73-78.	Flower	Hexane	Terpenoids	Lanosterol and isomers	-	-	GC-MS
Oliveira et al. (2014)	Fruit	Hexane	Terpenoid	Lanosterol	-	-	GC-MS
Silva & Paiva (2012)SILVA MCA & PAIVA SR. 2012. Antioxidant activity and flavonoid content of Clusia fluminensis Planch. & Triana. An Acad Bras Cienc 84: 609-616.	Fruit	Acetone	Flavonoids	-	13.93 ± 0.21	%	Colorimetric (415 nm)
	Stem	Acetone		-	9.12 ± 1.14	%
	Fruit	Methanol		-	10.68 ± 0.58	%
	Stem			-	9.82 ± 0.53	%
	Leaves			-	8.07 ± 1.70	%
Silva et al. (2012)SILVA MCA, HERINGER AP, FIGUEIREDO MR & PAIVA SR. 2012. Separation of clusianone from Clusia fluminensis Planch. and Triana (Clusiaceae) by high speed counter-current chromatography (HSCCC). J Liq Chromatogr Relat Technol 35: 2313-2321.	Flower	Hexane	Polyisoprenylated benzophenone	Clusianone tautomeric pair	6.9 yield	%	GC/MS
Porto et al. (2001)	Flower resin	Fresh material methylation with diazomethane a- diethyl ether	Polyisoprenylated benzophenones	Clusianone	37	%	RP-HPLC
				Spiritone	10	%
				Weddellianone/ Lanceolatone	6.7	%
Nogueira et al. (2001)NOGUEIRA PCL, BITTRICH V, SHEPHERD GJ, LOPES AV & MARSAIOLI AJ. 2001. The ecological and taxonomic importance of flower volatiles of Clusia species (Guttiferae). Phytochemistry 56: 443-452.	Flower petals essential oils	Fresh material distillation water with dichloromethane	Terpenoids	Sesquiterpenes	64.1	%	GC-MS
				Oxygen-containng sesquiterpenes	29.4	%
				Monoterpenes	0.5	%
				Oxygen-containng monoterpenes	0.1	%
			Carboxylic acids	Carboxylic acids	2	%	GC-MS
			Long chain hydrocarbons	Oxygen-containing long chain hydrocarbons	0.2	%	GC-MS
			Long chain hydrocarbons	Long chain hydrocarbons	0.1	%	GC-MS
Nagem et al. (1993)NAGEM TJ, MESQUITA AAL & SILVA R. 1993. Constituints of Clusia fluminensis. Fitoterapia LXIV: 380-381.	Leaves	-	Triterpenoids	Lupenone	640	µg / g	-
				Amyrin	617.14	µg / g
				α and- β friedelinol	328.57	µg / g
				Friedelin	71.42	µg / g
			Steroid	Sitosterol	457.14	µg / g
			Alcohol of fatty acid	n-octacosanol	257.14	µg / g
			Long chain hydrocarbons	Tricosane	642.86	µg / g

Biological Effect		Hexane				Dichloromethane	Acetone		Methanol			Water			Isolated compounds
Biological Effect		Leaves	Flower	Fruit	Stem	Flower	Fruit	Stem	Leaves	Fruit	Stem	Leaves	Fruit	Stem	Clusianone	Lanosterol
Anti-viral*	HSV-1 Inhibition	√	√	√	√	-	√	√	√	√	√	-	-	-	√	√
Anti-viral*	HIV-RT Inhibition	Ø	-	Ø	Ø	-	-	Ø	√	Ø	√	-	-	-	√	√
Insecticidal**	Aedes aegypti	-	√	Ø	-	-	-	-	-	-	-	-	-	-	√	Ø
	Dysdercus peruvianus	-	√	√	-	-	-	-	-	-	-	-	-	-	√	√
	Oncopeltus fasciatus	-	√	√		-	-	-	-	-	-	-	-	-	√	√
Snake venom antidote ***	Bothrops jararaca	√	√	√	√	√	√	√	√	√	√	√	√	√	√	√
Snake venom antidote ***	Bothrops jararacussu	-	-	-	-	-	-	-	-	-	-	√	√	√	-	-

Protocol	Biological Assay *()**	Model	Administration Route / Venom:plant ratio (w:w) ()**	Leaf			Stem				Fruit				Flower
Protocol	Biological Assay *()**	Model	Administration Route / Venom:plant ratio (w:w) ()**	Hex	MeOH	H ₂ O	Hex	Acet	MeOH	H ₂ O	Hex	Acet	MeOH	H ₂ O	Hex	CH ₂ Cl ₂
Pre-incubation Protocol	Proteolysis Reduction (%)	Bja	NA / 1:20	44	52	90	34	78	91	40	19	100	100	100	75	47
	Proteolysis Reduction (%)	Bju	NA / 1:20	-	-	58	-	-	-	28	-	-	-	100	-	-
	Hemolysis Reduction (%)	Bja	NA / 1:20	74	71	50	41	93	99	22	24	32	59	100	42	9
	Clotting Times (sec)	Bja	NA / 1:20	84	85	60	73	171	150	89	89	107	100	100	107	96
	Clotting Times (sec)	Bju	NA/ 1:5	-	-	70	-	-	-	76	-	-	-	82	-	-
	Hemorrhage Reduction (%)	Bja	i.d. / 1:2, 1:5 or 1:20(^c)	Ø	Ø	58	Ø	Ø	Ø	24	50	100	Ø	100	Ø	Ø
	Hemorrhage Reduction (%)	Bju	i.d. / 1:20	-	-	74	-	-	-	100	-	-	-	100	-	-
	Edema Reduction (%)	Bja	s.c. / 1:10	-	-	84	-	-	-	80	-	-	-	80	-	-
	Edema Reduction (%)	Bju	s.c. / 1:10	-	-	7	-	-	-	63	-	-	-	100	-	-
	Miotoxicity Reduction (CK Units)(^a)	Bju	i.m. / 1:10	-	-	1400	-	-	-	920	-	-	-	1360	-	-
	Survival Time (min)(^b)	Bja	i.p.; i.v./ 1:1	-	-	360 ± 3	-	-	-	360 ± 5	-	-	-	360 ± 4	-	-
	Survival Time (min)(^b)	Bju	i.v. / 1:1	-	-	145 ± 4	-	-	-	72 ± 7	-	-	-	360 ± 2	-	-
Treatment Protocol	Edema Reduction (%)	Bja	p.o. / 1:10	-	-	0	-	-	-	40	-	-	-	25	-	-
	Edema Reduction (%)	Bju	p.o. / 1:10	-	-	16	-	-	-	39	-	-	-	32	-	-
	Survival Time (min)	Bja	i.p./ 1:1 or 1:10(^d)	-	-	75 ± 0.7	-	900	900	180 ± 0.9	-	-	-	70 ± 0.6	-	-
	Survival Time (min)	Bju	iv / 1:1	-	-	70 ± 9	-	-	-	70 ± 6	-	-	-	360 ± 4	-	-
	Hemorrhage Reduction (%)	Bja	i.v. / 1:20	-	-	51	-	-	-	60	-	-	-	41	-	-
			s.c or i.d./ 1:2 or 1:20(^e)	-	-	51	-	-	-	60	10	10	-	41	-	-
			topical	-	-	-	-	-	-	-	-	-	-	50	-	-
		Bju	i.v. / 1:20	-	-	35	-	-	-	45	-	-	-	36	-	-
			s.c. / 1:20	-	-	35	-	-	-	45	-	-	-	36	-	-
			topical	-	-	-	-	-	-	-	-	-	-	55	-	-
Prevention Protocol	Hemorrhage Reduction (%)	Bja	p.o. / 1:20	-	-	42	-	-	-	Ø	-	-	-	43	-	-
Prevention Protocol	Hemorrhage Reduction (%)	Bju	p.o. / 1:20	-	-	46	-	-	-	50	-	-	-	35	-	-

[1] Correspondence to: Lídia Amorim E-mail: amorimlidia@id.uff.br

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The bioprospecting potential of Clusia fluminensis Planch. & Triana: a scoping review

Abstract